EyeLink Non-Human Primate Publications
All EyeLink non-human primate research publications up until 2019 (with some early 2020s) are listed below by year. You can search the publications using key words such as Temporal Cortex, Macaque, Antisaccade, etc. You can also search for individual author names. If we missed any EyeLink non-human primate article, please email us!
All EyeLink non-human primatee publications are also available for download / import into reference management software as a single Bibtex (.bib) file.
2020 |
Ramina Adam; Kevin Johnston; Ravi S Menon; Stefan Everling Functional reorganization during the recovery of contralesional target selection deficits after prefrontal cortex lesions in macaque monkeys Journal Article NeuroImage, 207 , pp. 1–17, 2020. @article{Adam2020, title = {Functional reorganization during the recovery of contralesional target selection deficits after prefrontal cortex lesions in macaque monkeys}, author = {Ramina Adam and Kevin Johnston and Ravi S Menon and Stefan Everling}, doi = {10.1016/j.neuroimage.2019.116339}, year = {2020}, date = {2020-01-01}, journal = {NeuroImage}, volume = {207}, pages = {1--17}, publisher = {Elsevier Ltd}, abstract = {Visual extinction has been characterized by the failure to respond to a visual stimulus in the contralesional hemifield when presented simultaneously with an ipsilesional stimulus (Corbetta and Shulman, 2011). Unilateral damage to the macaque frontoparietal cortex commonly leads to deficits in contralesional target selection that resemble visual extinction. Recently, we showed that macaque monkeys with unilateral lesions in the caudal prefrontal cortex (PFC) exhibited contralesional target selection deficits that recovered over 2–4 months (Adam et al., 2019). Here, we investigated the longitudinal changes in functional connectivity (FC) of the frontoparietal network after a small or large right caudal PFC lesion in four macaque monkeys. We collected ultra-high field resting-state fMRI at 7-T before the lesion and at weeks 1–16 post-lesion and compared the functional data with behavioural performance on a free-choice saccade task. We found that the pattern of frontoparietal network FC changes depended on lesion size, such that the recovery of contralesional extinction was associated with an initial increase in network FC that returned to baseline in the two small lesion monkeys, whereas FC continued to increase throughout recovery in the two monkeys with a larger lesion. We also found that the FC between contralesional dorsolateral PFC and ipsilesional parietal cortex correlated with behavioural recovery and that the contralesional dorsolateral PFC showed increasing degree centrality with the frontoparietal network. These findings suggest that both the contralesional and ipsilesional hemispheres play an important role in the recovery of function. Importantly, optimal compensation after large PFC lesions may require greater recruitment of distant and intact areas of the frontoparietal network, whereas recovery from smaller lesions was supported by a normalization of the functional network.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual extinction has been characterized by the failure to respond to a visual stimulus in the contralesional hemifield when presented simultaneously with an ipsilesional stimulus (Corbetta and Shulman, 2011). Unilateral damage to the macaque frontoparietal cortex commonly leads to deficits in contralesional target selection that resemble visual extinction. Recently, we showed that macaque monkeys with unilateral lesions in the caudal prefrontal cortex (PFC) exhibited contralesional target selection deficits that recovered over 2–4 months (Adam et al., 2019). Here, we investigated the longitudinal changes in functional connectivity (FC) of the frontoparietal network after a small or large right caudal PFC lesion in four macaque monkeys. We collected ultra-high field resting-state fMRI at 7-T before the lesion and at weeks 1–16 post-lesion and compared the functional data with behavioural performance on a free-choice saccade task. We found that the pattern of frontoparietal network FC changes depended on lesion size, such that the recovery of contralesional extinction was associated with an initial increase in network FC that returned to baseline in the two small lesion monkeys, whereas FC continued to increase throughout recovery in the two monkeys with a larger lesion. We also found that the FC between contralesional dorsolateral PFC and ipsilesional parietal cortex correlated with behavioural recovery and that the contralesional dorsolateral PFC showed increasing degree centrality with the frontoparietal network. These findings suggest that both the contralesional and ipsilesional hemispheres play an important role in the recovery of function. Importantly, optimal compensation after large PFC lesions may require greater recruitment of distant and intact areas of the frontoparietal network, whereas recovery from smaller lesions was supported by a normalization of the functional network. |
Ziad M Hafed; Laurent Goffart Gaze direction as equilibrium: More evidence from spatial and temporal aspects of small-saccade triggering in the rhesus macaque monkey Journal Article Journal of Neurophysiology, 123 (1), pp. 308–322, 2020. @article{Hafed2020, title = {Gaze direction as equilibrium: More evidence from spatial and temporal aspects of small-saccade triggering in the rhesus macaque monkey}, author = {Ziad M Hafed and Laurent Goffart}, doi = {10.1152/jn.00588.2019}, year = {2020}, date = {2020-01-01}, journal = {Journal of Neurophysiology}, volume = {123}, number = {1}, pages = {308--322}, abstract = {Rigorous behavioral studies made in human subjects have shown that small-eccentricity target displacements are associated with increased saccadic reaction times, but the reasons for this remain unclear. Before characterizing the neurophysiological foundations underlying this relationship between the spatial and temporal aspects of saccades, we tested the triggering of small saccades in the male rhesus macaque monkey. We also compared our results to those obtained in human subjects, both from the existing literature and through our own additional measurements. Using a variety of behavioral tasks exercising visual and nonvisual guidance of small saccades, we found that small saccades consistently require more time than larger saccades to be triggered in the nonhuman primate, even in the absence of any visual guidance and when valid advance information about the saccade landing position is available. We also found a strong asymmetry in the reaction times of small upper versus lower visual field visually guided saccades, a phenomenon that has not been described before for small saccades, even in humans. Following the suggestion that an eye movement is not initiated as long as the visuo-oculomotor system is within a state of balance, in which opposing commands counterbalance each other, we propose that the longer reaction times are a signature of enhanced times needed to create the symmetry-breaking condition that puts downstream premotor neurons into a push-pull regime necessary for rotating the eyeballs. Our results provide an important catalog of nonhuman primate oculomotor capabilities on the miniature scale, allowing concrete predictions on underlying neurophysiological mechanisms.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Rigorous behavioral studies made in human subjects have shown that small-eccentricity target displacements are associated with increased saccadic reaction times, but the reasons for this remain unclear. Before characterizing the neurophysiological foundations underlying this relationship between the spatial and temporal aspects of saccades, we tested the triggering of small saccades in the male rhesus macaque monkey. We also compared our results to those obtained in human subjects, both from the existing literature and through our own additional measurements. Using a variety of behavioral tasks exercising visual and nonvisual guidance of small saccades, we found that small saccades consistently require more time than larger saccades to be triggered in the nonhuman primate, even in the absence of any visual guidance and when valid advance information about the saccade landing position is available. We also found a strong asymmetry in the reaction times of small upper versus lower visual field visually guided saccades, a phenomenon that has not been described before for small saccades, even in humans. Following the suggestion that an eye movement is not initiated as long as the visuo-oculomotor system is within a state of balance, in which opposing commands counterbalance each other, we propose that the longer reaction times are a signature of enhanced times needed to create the symmetry-breaking condition that puts downstream premotor neurons into a push-pull regime necessary for rotating the eyeballs. Our results provide an important catalog of nonhuman primate oculomotor capabilities on the miniature scale, allowing concrete predictions on underlying neurophysiological mechanisms. |
2019 |
Ariana R Andrei; Sorin Pojoga; Roger Janz; Valentin Dragoi Integration of cortical population signals for visual perception Journal Article Nature Communications, 10 (1), pp. 1–13, 2019. @article{Andrei2019, title = {Integration of cortical population signals for visual perception}, author = {Ariana R Andrei and Sorin Pojoga and Roger Janz and Valentin Dragoi}, doi = {10.1038/s41467-019-11736-2}, year = {2019}, date = {2019-12-01}, journal = {Nature Communications}, volume = {10}, number = {1}, pages = {1--13}, publisher = {Nature Publishing Group}, abstract = {Visual stimuli evoke heterogeneous responses across nearby neural populations. These signals must be locally integrated to contribute to perception, but the principles underlying this process are unknown. Here, we exploit the systematic organization of orientation preference in macaque primary visual cortex (V1) and perform causal manipulations to examine the limits of signal integration. Optogenetic stimulation and visual stimuli are used to simultaneously drive two neural populations with overlapping receptive fields. We report that optogenetic stimulation raises firing rates uniformly across conditions, but improves the detection of visual stimuli only when activating cells that are preferentially-tuned to the visual stimulus. Further, we show that changes in correlated variability are exclusively present when the optogenetically and visually-activated populations are functionally-proximal, suggesting that correlation changes represent a hallmark of signal integration. Our results demonstrate that information from functionally-proximal neurons is pooled for perception, but functionally-distal signals remain independent. Primary visual cortical neurons exhibit diverse responses to visual stimuli yet how these signals are integrated during visual perception is not well understood. Here, the authors show that optogenetic stimulation of neurons situated near the visually‐driven population leads to improved orientation detection in monkeys through changes in correlated variability.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual stimuli evoke heterogeneous responses across nearby neural populations. These signals must be locally integrated to contribute to perception, but the principles underlying this process are unknown. Here, we exploit the systematic organization of orientation preference in macaque primary visual cortex (V1) and perform causal manipulations to examine the limits of signal integration. Optogenetic stimulation and visual stimuli are used to simultaneously drive two neural populations with overlapping receptive fields. We report that optogenetic stimulation raises firing rates uniformly across conditions, but improves the detection of visual stimuli only when activating cells that are preferentially-tuned to the visual stimulus. Further, we show that changes in correlated variability are exclusively present when the optogenetically and visually-activated populations are functionally-proximal, suggesting that correlation changes represent a hallmark of signal integration. Our results demonstrate that information from functionally-proximal neurons is pooled for perception, but functionally-distal signals remain independent. Primary visual cortical neurons exhibit diverse responses to visual stimuli yet how these signals are integrated during visual perception is not well understood. Here, the authors show that optogenetic stimulation of neurons situated near the visually‐driven population leads to improved orientation detection in monkeys through changes in correlated variability. |
Maria C Romero; Marco Davare; Marcelo Armendariz; Peter Janssen Neural effects of transcranial magnetic stimulation at the single-cell level Journal Article Nature Communications, 10 (1), pp. 1–11, 2019. @article{Romero2019, title = {Neural effects of transcranial magnetic stimulation at the single-cell level}, author = {Maria C Romero and Marco Davare and Marcelo Armendariz and Peter Janssen}, doi = {10.1038/s41467-019-10638-7}, year = {2019}, date = {2019-12-01}, journal = {Nature Communications}, volume = {10}, number = {1}, pages = {1--11}, publisher = {Nature Publishing Group}, abstract = {Transcranial magnetic stimulation (TMS) can non-invasively modulate neural activity in humans. Despite three decades of research, the spatial extent of the cortical area activated by TMS is still controversial. Moreover, how TMS interacts with task-related activity during motor behavior is unknown. Here, we applied single-pulse TMS over macaque parietal cortex while recording single-unit activity at various distances from the center of stimulation during grasping. The spatial extent of TMS-induced activation is remarkably restricted, affecting the spiking activity of single neurons in an area of cortex measuring less than 2 mm in diameter. In task-related neurons, TMS evokes a transient excitation followed by reduced activity, paralleled by a significantly longer grasping time. Furthermore, TMS-induced activity and task-related activity do not summate in single neurons. These results furnish crucial experimental evidence for the neural effects of TMS at the single-cell level and uncover the neural underpinnings of behavioral effects of TMS.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Transcranial magnetic stimulation (TMS) can non-invasively modulate neural activity in humans. Despite three decades of research, the spatial extent of the cortical area activated by TMS is still controversial. Moreover, how TMS interacts with task-related activity during motor behavior is unknown. Here, we applied single-pulse TMS over macaque parietal cortex while recording single-unit activity at various distances from the center of stimulation during grasping. The spatial extent of TMS-induced activation is remarkably restricted, affecting the spiking activity of single neurons in an area of cortex measuring less than 2 mm in diameter. In task-related neurons, TMS evokes a transient excitation followed by reduced activity, paralleled by a significantly longer grasping time. Furthermore, TMS-induced activity and task-related activity do not summate in single neurons. These results furnish crucial experimental evidence for the neural effects of TMS at the single-cell level and uncover the neural underpinnings of behavioral effects of TMS. |
Jacob A Westerberg; Alexander Maier; Geoffrey F Woodman; Jeffrey D Schall Performance monitoring during visual priming Journal Article Journal of Cognitive Neuroscience, pp. 1–12, 2019. @article{Westerberg2019a, title = {Performance monitoring during visual priming}, author = {Jacob A Westerberg and Alexander Maier and Geoffrey F Woodman and Jeffrey D Schall}, doi = {10.1162/jocn_a_01499}, year = {2019}, date = {2019-11-01}, journal = {Journal of Cognitive Neuroscience}, pages = {1--12}, publisher = {MIT Press - Journals}, abstract = {Repetitive performance of single-feature (efficient or pop-out) visual search improves RTs and accuracy. This phenomenon, known as priming of pop-out, has been demonstrated in both humans and macaque monkeys. We investigated the relationship between performance monitoring and priming of pop-out. Neuronal activity in the supplementary eye field (SEF) contributes to performance monitoring and to the generation of performance monitoring signals in the EEG. To determine whether priming depends on performance monitoring, we investigated spiking activity in SEF as well as the concurrent EEG of two monkeys performing a priming of pop-out task. We found that SEF spiking did not modulate with priming. Surprisingly, concurrent EEG did covary with priming. Together, these results suggest that performance monitoring contributes to priming of pop-out. However, this performance monitoring seems not mediated by SEF. This dissociation suggests that EEG indices of performance monitoring arise from multiple, functionally distinct neural generators.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Repetitive performance of single-feature (efficient or pop-out) visual search improves RTs and accuracy. This phenomenon, known as priming of pop-out, has been demonstrated in both humans and macaque monkeys. We investigated the relationship between performance monitoring and priming of pop-out. Neuronal activity in the supplementary eye field (SEF) contributes to performance monitoring and to the generation of performance monitoring signals in the EEG. To determine whether priming depends on performance monitoring, we investigated spiking activity in SEF as well as the concurrent EEG of two monkeys performing a priming of pop-out task. We found that SEF spiking did not modulate with priming. Surprisingly, concurrent EEG did covary with priming. Together, these results suggest that performance monitoring contributes to priming of pop-out. However, this performance monitoring seems not mediated by SEF. This dissociation suggests that EEG indices of performance monitoring arise from multiple, functionally distinct neural generators. |
Seth W Egger; Evan D Remington; Chia-Jung Chang; Mehrdad Jazayeri Internal models of sensorimotor integration regulate cortical dynamics Journal Article Nature Neuroscience, 22 , pp. 1871–1882, 2019. @article{Egger2019, title = {Internal models of sensorimotor integration regulate cortical dynamics}, author = {Seth W Egger and Evan D Remington and Chia-Jung Chang and Mehrdad Jazayeri}, doi = {10.1038/s41593-019-0500-6}, year = {2019}, date = {2019-10-01}, journal = {Nature Neuroscience}, volume = {22}, pages = {1871--1882}, publisher = {Springer Science and Business Media LLC}, abstract = {Sensorimotor control during overt movements is characterized in terms of three building blocks: a controller, a simulator and a state estimator. We asked whether the same framework could explain the control of internal states in the absence of movements. Recently, it was shown that the brain controls the timing of future movements by adjusting an internal speed command. We trained monkeys in a novel task in which the speed command had to be dynamically controlled based on the timing of a sequence of flashes. Recordings from the frontal cortex provided evidence that the brain updates the internal speed command after each flash based on the error between the timing of the flash and the anticipated timing of the flash derived from a simulated motor plan. These findings suggest that cognitive control of internal states may be understood in terms of the same computational principles as motor control. Control of movements can be understood in terms of the interplay between a controller, a simulator and an estimator. Egger et. al. show that cortical neurons establish the same building blocks to control cognitive states in the absence of movement.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Sensorimotor control during overt movements is characterized in terms of three building blocks: a controller, a simulator and a state estimator. We asked whether the same framework could explain the control of internal states in the absence of movements. Recently, it was shown that the brain controls the timing of future movements by adjusting an internal speed command. We trained monkeys in a novel task in which the speed command had to be dynamically controlled based on the timing of a sequence of flashes. Recordings from the frontal cortex provided evidence that the brain updates the internal speed command after each flash based on the error between the timing of the flash and the anticipated timing of the flash derived from a simulated motor plan. These findings suggest that cognitive control of internal states may be understood in terms of the same computational principles as motor control. Control of movements can be understood in terms of the interplay between a controller, a simulator and an estimator. Egger et. al. show that cortical neurons establish the same building blocks to control cognitive states in the absence of movement. |
Ramina Adam; Kevin Johnston; Stefan Everling Journal of Neurophysiology, 122 (2), pp. 672–690, 2019. @article{Adam2019, title = {Recovery of contralesional saccade choice and reaction time deficits after a unilateral endothelin-1-induced lesion in the macaque caudal prefrontal cortex}, author = {Ramina Adam and Kevin Johnston and Stefan Everling}, doi = {10.1152/jn.00078.2019}, year = {2019}, date = {2019-08-01}, journal = {Journal of Neurophysiology}, volume = {122}, number = {2}, pages = {672--690}, publisher = {American Physiological Society Bethesda, MD}, abstract = {The caudal primate prefrontal cortex (PFC) is involved in target selection and visually guided saccades through both covert attention and overt orienting eye movements. Unilateral damage to the caudal PFC often leads to decreased awareness of a contralesional target alone, referred to as “neglect,” or when it is presented simultaneously with an ipsilesional target, referred to as “extinction.” In the current study, we examined whether deficits in contralesional target selection were due to contralesional oculomotor deficits, such as slower reaction times. We experimentally induced a focal ischemic lesion in the right caudal PFC of 4 male macaque monkeys using the vasoconstrictor endothelin-1 and measured saccade choice and reaction times on double-stimulus free-choice tasks and single-stimulus trials before and after the lesion. We found that 1) endothelin-1-induced lesions in the caudal PFC produced contralesional target selection deficits that varied in severity and duration based on lesion volume and location; 2) contralesional neglect-like deficits were transient and recovered by week 4 postlesion; 3) contralesional extinction-like deficits were longer lasting and recovered by weeks 8–16 postlesion; 4) contralesional reaction time returned to baseline well before the contralesional choice deficit had recovered; and 5) neither the mean reaction times nor the reaction time distributions could account for the degree of contralesional extinction on the free-choice task throughout recovery. These findings demonstrate that the saccade choice bias observed after a right caudal PFC lesion is not exclusively due to contralesional motor deficits, but instead reflects a combination of impaired motor and attentional processing.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The caudal primate prefrontal cortex (PFC) is involved in target selection and visually guided saccades through both covert attention and overt orienting eye movements. Unilateral damage to the caudal PFC often leads to decreased awareness of a contralesional target alone, referred to as “neglect,” or when it is presented simultaneously with an ipsilesional target, referred to as “extinction.” In the current study, we examined whether deficits in contralesional target selection were due to contralesional oculomotor deficits, such as slower reaction times. We experimentally induced a focal ischemic lesion in the right caudal PFC of 4 male macaque monkeys using the vasoconstrictor endothelin-1 and measured saccade choice and reaction times on double-stimulus free-choice tasks and single-stimulus trials before and after the lesion. We found that 1) endothelin-1-induced lesions in the caudal PFC produced contralesional target selection deficits that varied in severity and duration based on lesion volume and location; 2) contralesional neglect-like deficits were transient and recovered by week 4 postlesion; 3) contralesional extinction-like deficits were longer lasting and recovered by weeks 8–16 postlesion; 4) contralesional reaction time returned to baseline well before the contralesional choice deficit had recovered; and 5) neither the mean reaction times nor the reaction time distributions could account for the degree of contralesional extinction on the free-choice task throughout recovery. These findings demonstrate that the saccade choice bias observed after a right caudal PFC lesion is not exclusively due to contralesional motor deficits, but instead reflects a combination of impaired motor and attentional processing. |
Kun Guo; Zhihan Li; Yin Yan; Wu Li Viewing heterospecific facial expressions: An eye-tracking study of human and monkey viewers Journal Article Experimental Brain Research, 237 , pp. 2045–2059, 2019. @article{Guo2019, title = {Viewing heterospecific facial expressions: An eye-tracking study of human and monkey viewers}, author = {Kun Guo and Zhihan Li and Yin Yan and Wu Li}, doi = {10.1007/s00221-019-05574-3}, year = {2019}, date = {2019-08-01}, journal = {Experimental Brain Research}, volume = {237}, pages = {2045--2059}, publisher = {Springer Berlin Heidelberg}, abstract = {Common facial expressions of emotion have distinctive patterns of facial muscle movements that are culturally similar among humans, and perceiving these expressions is associated with stereotypical gaze allocation at local facial regions that are characteristic for each expression, such as eyes in angry faces. It is, however, unclear to what extent this ‘universality' view can be extended to process heterospecific facial expressions, and how ‘social learning' process contributes to heterospecific expression perception. In this eye-tracking study, we examined face-viewing gaze allocation of human (including dog owners and non-dog owners) and monkey observers while exploring expressive human, chimpanzee, monkey and dog faces (positive, neutral and negative expressions in human and dog faces; neutral and negative expressions in chimpanzee and monkey faces). Human observers showed species- and experience-dependent expression categorization accuracy. Furthermore, both human and monkey observers demonstrated different face-viewing gaze distributions which were also species dependent. Specifically, humans predominately attended at human eyes but animal mouth when judging facial expressions. Monkeys' gaze distributions in exploring human and monkey faces were qualitatively different from exploring chimpanzee and dog faces. Interestingly, the gaze behaviour of both human and monkey observers were further affected by their prior experience of the viewed species. It seems that facial expression processing is species dependent, and social learning may play a significant role in discriminating even rudimentary types of heterospecific expressions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Common facial expressions of emotion have distinctive patterns of facial muscle movements that are culturally similar among humans, and perceiving these expressions is associated with stereotypical gaze allocation at local facial regions that are characteristic for each expression, such as eyes in angry faces. It is, however, unclear to what extent this ‘universality' view can be extended to process heterospecific facial expressions, and how ‘social learning' process contributes to heterospecific expression perception. In this eye-tracking study, we examined face-viewing gaze allocation of human (including dog owners and non-dog owners) and monkey observers while exploring expressive human, chimpanzee, monkey and dog faces (positive, neutral and negative expressions in human and dog faces; neutral and negative expressions in chimpanzee and monkey faces). Human observers showed species- and experience-dependent expression categorization accuracy. Furthermore, both human and monkey observers demonstrated different face-viewing gaze distributions which were also species dependent. Specifically, humans predominately attended at human eyes but animal mouth when judging facial expressions. Monkeys' gaze distributions in exploring human and monkey faces were qualitatively different from exploring chimpanzee and dog faces. Interestingly, the gaze behaviour of both human and monkey observers were further affected by their prior experience of the viewed species. It seems that facial expression processing is species dependent, and social learning may play a significant role in discriminating even rudimentary types of heterospecific expressions. |
Guillaume Doucet; Roberto A Gulli; Benjamin W Corrigan; Lyndon R Duong; Julio C Martinez‐Trujillo Modulation of local field potentials and neuronal activity in primate hippocampus during saccades Journal Article Hippocampus, pp. 1–18, 2019. @article{Doucet2019, title = {Modulation of local field potentials and neuronal activity in primate hippocampus during saccades}, author = {Guillaume Doucet and Roberto A Gulli and Benjamin W Corrigan and Lyndon R Duong and Julio C Martinez‐Trujillo}, doi = {10.1002/hipo.23140}, year = {2019}, date = {2019-07-01}, journal = {Hippocampus}, pages = {1--18}, publisher = {Wiley}, abstract = {Primates use saccades to gather information about objects and their relative spatial arrangement, a process essential for visual perception and memory. It has been proposed that signals linked to saccades reset the phase of local field potential (LFP) oscillations in the hippocampus, providing a temporal window for visual signals to activate neurons in this region and influence memory formation. We investigated this issue by measuring hippocampal LFPs and spikes in two macaques performing different tasks with unconstrained eye movements. We found that LFP phase clustering (PC) in the alpha/beta (8-16 Hz) frequencies followed foveation onsets, while PC in frequencies lower than 8 Hz followed spontaneous saccades, even on a homogeneous background. Saccades to a solid grey background were not followed by increases in local neuronal firing, whereas saccades toward appearing visual stimuli were. Finally, saccade parameters correlated with LFPs phase and amplitude: saccade direction correlated with delta (≤4 Hz) phase, and saccade amplitude with theta (4-8 Hz) power. Our results suggest that signals linked to saccades reach the hippocampus, producing synchronization of delta/theta LFPs without a general activation of local neurons. Moreover, some visual inputs co-occurring with saccades produce LFP synchronization in the alpha/beta bands and elevated neuronal firing. Our findings support the hypothesis that saccade-related signals enact sensory input-dependent plasticity and therefore memory formation in the primate hippocampus.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Primates use saccades to gather information about objects and their relative spatial arrangement, a process essential for visual perception and memory. It has been proposed that signals linked to saccades reset the phase of local field potential (LFP) oscillations in the hippocampus, providing a temporal window for visual signals to activate neurons in this region and influence memory formation. We investigated this issue by measuring hippocampal LFPs and spikes in two macaques performing different tasks with unconstrained eye movements. We found that LFP phase clustering (PC) in the alpha/beta (8-16 Hz) frequencies followed foveation onsets, while PC in frequencies lower than 8 Hz followed spontaneous saccades, even on a homogeneous background. Saccades to a solid grey background were not followed by increases in local neuronal firing, whereas saccades toward appearing visual stimuli were. Finally, saccade parameters correlated with LFPs phase and amplitude: saccade direction correlated with delta (≤4 Hz) phase, and saccade amplitude with theta (4-8 Hz) power. Our results suggest that signals linked to saccades reach the hippocampus, producing synchronization of delta/theta LFPs without a general activation of local neurons. Moreover, some visual inputs co-occurring with saccades produce LFP synchronization in the alpha/beta bands and elevated neuronal firing. Our findings support the hypothesis that saccade-related signals enact sensory input-dependent plasticity and therefore memory formation in the primate hippocampus. |
Florian Sandhaeger; Constantin von Nicolai; Earl K Miller; Markus Siegel Monkey EEG links neuronal color and motion information across species and scales Journal Article eLife, 8 , pp. 1–21, 2019. @article{Sandhaeger2019, title = {Monkey EEG links neuronal color and motion information across species and scales}, author = {Florian Sandhaeger and Constantin von Nicolai and Earl K Miller and Markus Siegel}, doi = {10.7554/elife.45645}, year = {2019}, date = {2019-07-01}, journal = {eLife}, volume = {8}, pages = {1--21}, publisher = {eLife Sciences Publications, Ltd}, abstract = {It remains challenging to relate EEG and MEG to underlying circuit processes and comparable experiments on both spatial scales are rare. To close this gap between invasive and non-invasive electrophysiology we developed and recorded human-comparable EEG in macaque monkeys during visual stimulation with colored dynamic random dot patterns. Furthermore, we performed simultaneous microelectrode recordings from 6 areas of macaque cortex and human MEG. Motion direction and color information were accessible in all signals. Tuning of the non-invasive signals was similar to V4 and IT, but not to dorsal and frontal areas. Thus, MEG and EEG were dominated by early visual and ventral stream sources. Source level analysis revealed corresponding information and latency gradients across cortex. We show how information-based methods and monkey EEG can identify analogous properties of visual processing in signals spanning spatial scales from single units to MEG – a valuable framework for relating human and animal studies. DOI:}, keywords = {}, pubstate = {published}, tppubtype = {article} } It remains challenging to relate EEG and MEG to underlying circuit processes and comparable experiments on both spatial scales are rare. To close this gap between invasive and non-invasive electrophysiology we developed and recorded human-comparable EEG in macaque monkeys during visual stimulation with colored dynamic random dot patterns. Furthermore, we performed simultaneous microelectrode recordings from 6 areas of macaque cortex and human MEG. Motion direction and color information were accessible in all signals. Tuning of the non-invasive signals was similar to V4 and IT, but not to dorsal and frontal areas. Thus, MEG and EEG were dominated by early visual and ventral stream sources. Source level analysis revealed corresponding information and latency gradients across cortex. We show how information-based methods and monkey EEG can identify analogous properties of visual processing in signals spanning spatial scales from single units to MEG – a valuable framework for relating human and animal studies. DOI: |
Marzyeh Azimi; Mariann Oemisch; Thilo Womelsdorf Psychopharmacology, pp. 1–14, 2019. @article{Azimi2019, title = {Dissociation of nicotinic $alpha$7 and $alpha$4/$beta$2 sub-receptor agonists for enhancing learning and attentional filtering in nonhuman primates}, author = {Marzyeh Azimi and Mariann Oemisch and Thilo Womelsdorf}, doi = {10.1007/s00213-019-05430-w}, year = {2019}, date = {2019-01-01}, journal = {Psychopharmacology}, pages = {1--14}, publisher = {Psychopharmacology}, abstract = {Rationale: Nicotinic acetylcholine receptors (nAChRs) modulate attention, memory, and higher executive functioning, but it is unclear how nACh sub-receptors mediate different mechanisms supporting these functions. Objectives: We investigated whether selective agonists for the alpha-7 nAChR versus the alpha-4/beta-2 nAChR have unique functional contributions for value learning and attentional filtering of distractors in the nonhuman primate. Methods: Two adult rhesus macaque monkeys performed reversal learning following systemic administration of either the alpha-7 nAChR agonist PHA-543613 or the alpha-4/beta-2 nAChR agonist ABT-089 or a vehicle control. Behavioral analysis quantified performance accuracy, speed of processing, reversal learning speed, the control of distractor interference, perseveration tendencies, and motivation. Results: We found that the alpha-7 nAChR agonist PHA-543613 enhanced the learning speed of feature values but did not modulate how salient distracting information was filtered from ongoing choice processes. In contrast, the selective alpha-4/beta-2 nAChR agonist ABT-089 did not affect learning speed but reduced distractibility. This dissociation was dose-dependent and evident in the absence of systematic changes in overall performance, reward intake, motivation to perform the task, perseveration tendencies, or reaction times. Conclusions: These results suggest nicotinic sub-receptor specific mechanisms consistent with (1) alpha-4/beta-2 nAChR specific amplification of cholinergic transients in prefrontal cortex linked to enhanced cue detection in light of interferences, and (2) alpha-7 nAChR specific activation prolonging cholinergic transients, which could facilitate subjects to follow-through with newly established attentional strategies when outcome contingencies change. These insights will be critical for developing function-specific drugs alleviating attention and learning deficits in neuro-psychiatric diseases.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Rationale: Nicotinic acetylcholine receptors (nAChRs) modulate attention, memory, and higher executive functioning, but it is unclear how nACh sub-receptors mediate different mechanisms supporting these functions. Objectives: We investigated whether selective agonists for the alpha-7 nAChR versus the alpha-4/beta-2 nAChR have unique functional contributions for value learning and attentional filtering of distractors in the nonhuman primate. Methods: Two adult rhesus macaque monkeys performed reversal learning following systemic administration of either the alpha-7 nAChR agonist PHA-543613 or the alpha-4/beta-2 nAChR agonist ABT-089 or a vehicle control. Behavioral analysis quantified performance accuracy, speed of processing, reversal learning speed, the control of distractor interference, perseveration tendencies, and motivation. Results: We found that the alpha-7 nAChR agonist PHA-543613 enhanced the learning speed of feature values but did not modulate how salient distracting information was filtered from ongoing choice processes. In contrast, the selective alpha-4/beta-2 nAChR agonist ABT-089 did not affect learning speed but reduced distractibility. This dissociation was dose-dependent and evident in the absence of systematic changes in overall performance, reward intake, motivation to perform the task, perseveration tendencies, or reaction times. Conclusions: These results suggest nicotinic sub-receptor specific mechanisms consistent with (1) alpha-4/beta-2 nAChR specific amplification of cholinergic transients in prefrontal cortex linked to enhanced cue detection in light of interferences, and (2) alpha-7 nAChR specific activation prolonging cholinergic transients, which could facilitate subjects to follow-through with newly established attentional strategies when outcome contingencies change. These insights will be critical for developing function-specific drugs alleviating attention and learning deficits in neuro-psychiatric diseases. |
Pragathi Priyadharsini Balasubramani; Meghan C Pesce; Benjamin Y Hayden Activity in orbitofrontal neuronal ensembles reflects inhibitory control Journal Article European Journal of Neuroscience, pp. 1–19, 2019. @article{Balasubramani2019, title = {Activity in orbitofrontal neuronal ensembles reflects inhibitory control}, author = {Pragathi Priyadharsini Balasubramani and Meghan C Pesce and Benjamin Y Hayden}, doi = {10.1111/ejn.14638}, year = {2019}, date = {2019-01-01}, journal = {European Journal of Neuroscience}, pages = {1--19}, abstract = {Stopping, or inhibition, is a form of self-control that is a core element of flexible and adaptive behavior. Its neural origins remain unclear. Some views hold that inhibition decisions reflect the aggregation of widespread and diverse pieces of information, including information arising in ostensible core reward regions (i.e., outside the canonical executive system). We recorded activity of single neurons in the orbitofrontal cortex (OFC) of macaques, a region associated with economic decisions, and whose role in inhibition is debated. Subjects performed a classic inhibition task known as the stop signal task. Ensemble decoding analyses reveal a clear firing rate pattern that distinguishes successful from failed inhibition and that begins after the stop signal and before the stop signal reaction time (SSRT). We also found a different and orthogonal ensemble pattern that distinguishes successful from failed stopping before the beginning of the trial. These signals were distinct from, and orthogonal to, value encoding, which was also observed in these neurons. The timing of the early and late signals was, respectively, consistent with the idea that neuronal activity in OFC encodes inhibition both proactively and reactively.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Stopping, or inhibition, is a form of self-control that is a core element of flexible and adaptive behavior. Its neural origins remain unclear. Some views hold that inhibition decisions reflect the aggregation of widespread and diverse pieces of information, including information arising in ostensible core reward regions (i.e., outside the canonical executive system). We recorded activity of single neurons in the orbitofrontal cortex (OFC) of macaques, a region associated with economic decisions, and whose role in inhibition is debated. Subjects performed a classic inhibition task known as the stop signal task. Ensemble decoding analyses reveal a clear firing rate pattern that distinguishes successful from failed inhibition and that begins after the stop signal and before the stop signal reaction time (SSRT). We also found a different and orthogonal ensemble pattern that distinguishes successful from failed stopping before the beginning of the trial. These signals were distinct from, and orthogonal to, value encoding, which was also observed in these neurons. The timing of the early and late signals was, respectively, consistent with the idea that neuronal activity in OFC encodes inhibition both proactively and reactively. |
Marie E Bellet; Joachim Bellet; Hendrikje Nienborg; Ziad M Hafed; Philipp Berens Human-level saccade detection performance using deep neural networks Journal Article Journal of Neurophysiology, 121 (2), pp. 646–661, 2019. @article{Bellet2019, title = {Human-level saccade detection performance using deep neural networks}, author = {Marie E Bellet and Joachim Bellet and Hendrikje Nienborg and Ziad M Hafed and Philipp Berens}, doi = {10.1152/jn.00601.2018}, year = {2019}, date = {2019-01-01}, journal = {Journal of Neurophysiology}, volume = {121}, number = {2}, pages = {646--661}, abstract = {Saccades are ballistic eye movements that rapidly shift gaze from one location of visual space to another. Detecting saccades in eye movement recordings is important not only for studying the neural mechanisms underlying sensory, motor, and cognitive processes, but also as a clinical and diagnostic tool. However, automatically detecting saccades can be difficult, particularly when such saccades are generated in coordination with other tracking eye movements, like smooth pursuits, or when the saccade amplitude is close to eye tracker noise levels, like with microsaccades. In such cases, labeling by human experts is required, but this is a tedious task prone to variability and error. We developed a convolutional neural network to automatically detect saccades at human-level accuracy and with minimal training examples. Our algorithm surpasses state of the art according to common performance metrics and could facilitate studies of neurophysiological processes underlying saccade generation and visual processing.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Saccades are ballistic eye movements that rapidly shift gaze from one location of visual space to another. Detecting saccades in eye movement recordings is important not only for studying the neural mechanisms underlying sensory, motor, and cognitive processes, but also as a clinical and diagnostic tool. However, automatically detecting saccades can be difficult, particularly when such saccades are generated in coordination with other tracking eye movements, like smooth pursuits, or when the saccade amplitude is close to eye tracker noise levels, like with microsaccades. In such cases, labeling by human experts is required, but this is a tedious task prone to variability and error. We developed a convolutional neural network to automatically detect saccades at human-level accuracy and with minimal training examples. Our algorithm surpasses state of the art according to common performance metrics and could facilitate studies of neurophysiological processes underlying saccade generation and visual processing. |
Narcisse P Bichot; Rui Xu; Azriel Ghadooshahy; Michael L Williams; Robert Desimone The role of prefrontal cortex in the control of feature attention in area V4 Journal Article Nature Communications, 10 , pp. 1–12, 2019. @article{Bichot2019, title = {The role of prefrontal cortex in the control of feature attention in area V4}, author = {Narcisse P Bichot and Rui Xu and Azriel Ghadooshahy and Michael L Williams and Robert Desimone}, doi = {10.1038/s41467-019-13761-7}, year = {2019}, date = {2019-01-01}, journal = {Nature Communications}, volume = {10}, pages = {1--12}, publisher = {Springer US}, abstract = {When searching for an object in a cluttered scene, we can use our memory of the target object features to guide our search, and the responses of neurons in multiple cortical visual areas are enhanced when their receptive field contains a stimulus sharing target object features. Here we tested the role of the ventral prearcuate region (VPA) of prefrontal cortex in the control of feature attention in cortical visual area V4. VPA was unilaterally inactivated in monkeys performing a free-viewing visual search for a target stimulus in an array of stimuli, impairing monkeys' ability to find the target in the array in the affected hemifield, but leaving intact their ability to make saccades to targets presented alone. Simultaneous recordings in V4 revealed that the effects of feature attention on V4 responses were eliminated or greatly reduced while leaving the effects of spatial attention on responses intact. Altogether, the results suggest that feedback from VPA modulates processing in visual cortex during attention to object features.}, keywords = {}, pubstate = {published}, tppubtype = {article} } When searching for an object in a cluttered scene, we can use our memory of the target object features to guide our search, and the responses of neurons in multiple cortical visual areas are enhanced when their receptive field contains a stimulus sharing target object features. Here we tested the role of the ventral prearcuate region (VPA) of prefrontal cortex in the control of feature attention in cortical visual area V4. VPA was unilaterally inactivated in monkeys performing a free-viewing visual search for a target stimulus in an array of stimuli, impairing monkeys' ability to find the target in the array in the affected hemifield, but leaving intact their ability to make saccades to targets presented alone. Simultaneous recordings in V4 revealed that the effects of feature attention on V4 responses were eliminated or greatly reduced while leaving the effects of spatial attention on responses intact. Altogether, the results suggest that feedback from VPA modulates processing in visual cortex during attention to object features. |
Rasmus M Birn; Alexander K Converse; Abigail Z Rajala; Andrew L Alexander; Walter F Block; Alan B McMillan; Bradley T Christian; Caitlynn N Filla; Dhanabalan Murali; Samuel A Hurley; Rick L Jenison; Luis C Populin Changes in endogenous dopamine induced by methylphenidate predict functional connectivity in nonhuman primates Journal Article The Journal of Neuroscience, 39 (8), pp. 1436–1444, 2019. @article{Birn2019, title = {Changes in endogenous dopamine induced by methylphenidate predict functional connectivity in nonhuman primates}, author = {Rasmus M Birn and Alexander K Converse and Abigail Z Rajala and Andrew L Alexander and Walter F Block and Alan B McMillan and Bradley T Christian and Caitlynn N Filla and Dhanabalan Murali and Samuel A Hurley and Rick L Jenison and Luis C Populin}, doi = {10.1523/JNEUROSCI.2513-18.2018}, year = {2019}, date = {2019-01-01}, journal = {The Journal of Neuroscience}, volume = {39}, number = {8}, pages = {1436--1444}, abstract = {Dopamine (DA) levels in the striatum are increased by many therapeutic drugs, such as methylphenidate (MPH), which also alters behavioral and cognitive functions thought to be controlled by the PFC dose-dependently. We linked DA changes and functional connectivity (FC) using simultaneous [18F]fallypride PET and resting-state fMRI in awake male rhesus monkeys after oral administration of various doses of MPH. We found a negative correlation between [18F]fallypride nondisplaceable binding potential (BPND) and MPH dose in the head of the caudate (hCd), demonstrating increased extracellular DA resulting from MPH administration. The decreased BPND was negatively correlated with FC between the hCd and the PFC. Subsequent voxelwise analyses revealed negative correlations with FC between the hCd and the dorsolateral PFC, hippocampus, and precuneus. These results, showing that MPH-induced changes in DA levels in the hCd predict resting-state FC, shed light on a mechanism by which changes in striatal DA could influence function in the PFC.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Dopamine (DA) levels in the striatum are increased by many therapeutic drugs, such as methylphenidate (MPH), which also alters behavioral and cognitive functions thought to be controlled by the PFC dose-dependently. We linked DA changes and functional connectivity (FC) using simultaneous [18F]fallypride PET and resting-state fMRI in awake male rhesus monkeys after oral administration of various doses of MPH. We found a negative correlation between [18F]fallypride nondisplaceable binding potential (BPND) and MPH dose in the head of the caudate (hCd), demonstrating increased extracellular DA resulting from MPH administration. The decreased BPND was negatively correlated with FC between the hCd and the PFC. Subsequent voxelwise analyses revealed negative correlations with FC between the hCd and the dorsolateral PFC, hippocampus, and precuneus. These results, showing that MPH-induced changes in DA levels in the hCd predict resting-state FC, shed light on a mechanism by which changes in striatal DA could influence function in the PFC. |
Amarender R Bogadhi; Anil Bollimunta; David A Leopold; Richard J Krauzlis Spatial attention deficits are causally linked to an area in macaque temporal cortex Journal Article Current Biology, 29 , pp. 726–736, 2019. @article{Bogadhi2019, title = {Spatial attention deficits are causally linked to an area in macaque temporal cortex}, author = {Amarender R Bogadhi and Anil Bollimunta and David A Leopold and Richard J Krauzlis}, doi = {10.1016/j.cub.2019.01.028}, year = {2019}, date = {2019-01-01}, journal = {Current Biology}, volume = {29}, pages = {726--736}, abstract = {Spatial neglect is a common clinical syndrome involving disruption of the brain's attention-related circuitry, including the dorsocaudal temporal cortex. In macaques, the attention deficits associated with neglect can be readily modeled, but the absence of evidence for temporal cortex involvement has suggested a fundamental difference from humans. To map the neurological expression of neglect-like attention deficits in macaques, we measured attention-related fMRI activity across the cerebral cortex during experimental induction of neglect through reversible inactivation of the superior colliculus and frontal eye fields. During inactivation, monkeys exhibited hallmark attentional deficits of neglect in tasks using either motion or non-motion stimuli. The behavioral deficits were accompanied by marked reductions in fMRI attentional modulation that were strongest in a small region on the floor of the superior temporal sulcus; smaller reductions were also found in frontal eye fields and dorsal parietal cortex. Notably, direct inactivation of the mid-superior temporal sulcus (STS) cortical region identified by fMRI caused similar neglect-like spatial attention deficits. These results identify a putative macaque homolog to temporal cortex structures known to play a central role in human neglect.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Spatial neglect is a common clinical syndrome involving disruption of the brain's attention-related circuitry, including the dorsocaudal temporal cortex. In macaques, the attention deficits associated with neglect can be readily modeled, but the absence of evidence for temporal cortex involvement has suggested a fundamental difference from humans. To map the neurological expression of neglect-like attention deficits in macaques, we measured attention-related fMRI activity across the cerebral cortex during experimental induction of neglect through reversible inactivation of the superior colliculus and frontal eye fields. During inactivation, monkeys exhibited hallmark attentional deficits of neglect in tasks using either motion or non-motion stimuli. The behavioral deficits were accompanied by marked reductions in fMRI attentional modulation that were strongest in a small region on the floor of the superior temporal sulcus; smaller reductions were also found in frontal eye fields and dorsal parietal cortex. Notably, direct inactivation of the mid-superior temporal sulcus (STS) cortical region identified by fMRI caused similar neglect-like spatial attention deficits. These results identify a putative macaque homolog to temporal cortex structures known to play a central role in human neglect. |
Xinying Cai; Camillo Padoa-Schioppa Neuronal evidence for good-based economic decisions under variable action costs Journal Article Nature Communications, 10 , pp. 1–13, 2019. @article{Cai2019, title = {Neuronal evidence for good-based economic decisions under variable action costs}, author = {Xinying Cai and Camillo Padoa-Schioppa}, doi = {10.1038/s41467-018-08209-3}, year = {2019}, date = {2019-01-01}, journal = {Nature Communications}, volume = {10}, pages = {1--13}, abstract = {Previous work showed that economic decisions can be made independently of spatial contingencies. However, when goods available for choice bear different action costs, the decision necessarily reflects aspects of the action. One possibility is that "stimulus values" are combined with the corresponding action costs in a motor representation, and decisions are then made in actions space. Alternatively, action costs could be integrated with other determinants of value in a non-spatial representation. If so, decisions under variable action costs could take place in goods space. Here, we recorded from orbitofrontal cortex while monkeys chose between different juices offered in variable amounts. We manipulated action costs by varying the saccade amplitude, and we dissociated in time and space offer presentation from action planning. Neurons encoding the binary choice outcome did so well before the presentation of saccade targets, indicating that decisions were made in goods space.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Previous work showed that economic decisions can be made independently of spatial contingencies. However, when goods available for choice bear different action costs, the decision necessarily reflects aspects of the action. One possibility is that "stimulus values" are combined with the corresponding action costs in a motor representation, and decisions are then made in actions space. Alternatively, action costs could be integrated with other determinants of value in a non-spatial representation. If so, decisions under variable action costs could take place in goods space. Here, we recorded from orbitofrontal cortex while monkeys chose between different juices offered in variable amounts. We manipulated action costs by varying the saccade amplitude, and we dissociated in time and space offer presentation from action planning. Neurons encoding the binary choice outcome did so well before the presentation of saccade targets, indicating that decisions were made in goods space. |
Katherine E Conen; X Camillo Padoa-Schioppa Partial adaptation to the value range in the macaque orbitofrontal cortex Journal Article The Journal of Neuroscience, 39 (18), pp. 3498 –3513, 2019. @article{Conen2019, title = {Partial adaptation to the value range in the macaque orbitofrontal cortex}, author = {Katherine E Conen and X {Camillo Padoa-Schioppa}}, doi = {10.1523/JNEUROSCI.2279-18.2019}, year = {2019}, date = {2019-01-01}, journal = {The Journal of Neuroscience}, volume = {39}, number = {18}, pages = {3498 --3513}, abstract = {Values available for choice in different behavioral contexts can vary immensely. To compensate for this variability, neuronal circuits underlying economic decisions undergo adaptation. In orbitofrontal cortex (OFC), neurons encode the subjective value of offered and chosen goods in a quasilinear way. Previous experiments found that the gain of the encoding is lower when the value range is wider. However, the parameters OFC neurons adapted to remained unclear. Furthermore, previous studies did not examine additive changes in neuronal responses. Computational considerations indicate that these factors can directly impact choice behavior. Here we investigated how OFC neurons adapt to changes in the value range. We recorded from two male rhesus monkeys during a juice choice task. Each session was divided into two blocks of trials. In each block, juices were offered within a set range of values, and ranges changed between blocks. Across blocks, neuronal responses adapted to both the maximum and the minimum value, but only partially. As a result, the minimum neural activity was elevated in some value ranges relative to others. Through simulation of a linear decision model, we showed that increasing the minimum response increases choice variability, lowering the expected payoff. This effect is modulated by the balance between cells with positive and negative encoding. The presence of these two populations induces a non-monotonic relationship between the value range and choice efficacy, such that the expected payoff is highest for decisions in an intermediate value range.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Values available for choice in different behavioral contexts can vary immensely. To compensate for this variability, neuronal circuits underlying economic decisions undergo adaptation. In orbitofrontal cortex (OFC), neurons encode the subjective value of offered and chosen goods in a quasilinear way. Previous experiments found that the gain of the encoding is lower when the value range is wider. However, the parameters OFC neurons adapted to remained unclear. Furthermore, previous studies did not examine additive changes in neuronal responses. Computational considerations indicate that these factors can directly impact choice behavior. Here we investigated how OFC neurons adapt to changes in the value range. We recorded from two male rhesus monkeys during a juice choice task. Each session was divided into two blocks of trials. In each block, juices were offered within a set range of values, and ranges changed between blocks. Across blocks, neuronal responses adapted to both the maximum and the minimum value, but only partially. As a result, the minimum neural activity was elevated in some value ranges relative to others. Through simulation of a linear decision model, we showed that increasing the minimum response increases choice variability, lowering the expected payoff. This effect is modulated by the balance between cells with positive and negative encoding. The presence of these two populations induces a non-monotonic relationship between the value range and choice efficacy, such that the expected payoff is highest for decisions in an intermediate value range. |
Michele A Cox; Kacie Dougherty; Geoffrey K Adams; Eric A Reavis; Jacob A Westerberg; Brandon S Moore; David A Leopold; Alexander Maier Spiking suppression precedes cued attentional enhancement of neural responses in primary visual cortex Journal Article Cerebral Cortex, 29 , pp. 77–90, 2019. @article{Cox2019a, title = {Spiking suppression precedes cued attentional enhancement of neural responses in primary visual cortex}, author = {Michele A Cox and Kacie Dougherty and Geoffrey K Adams and Eric A Reavis and Jacob A Westerberg and Brandon S Moore and David A Leopold and Alexander Maier}, doi = {10.1093/cercor/bhx305}, year = {2019}, date = {2019-01-01}, journal = {Cerebral Cortex}, volume = {29}, pages = {77--90}, abstract = {Attending to a visual stimulus increases its detectability, even if gaze is directed elsewhere. This covert attentional selection is known to enhance spiking across many brain areas, including the primary visual cortex (V1). Here we investigate the temporal dynamics of attention-related spiking changes in V1 of macaques performing a task that separates attentional selection from the onset of visual stimulation. We found that preceding attentional enhancement there was a sharp, transient decline in spiking following presentation of an attention-guiding cue. This disruption of V1 spiking was not observed in a task-naive subject that passively observed the same stimulus sequence, suggesting that sensory activation is insufficient to cause suppression. Following this suppression, attended stimuli evoked more spiking than unattended stimuli, matching previous reports of attention-related activity in V1. Laminar analyses revealed a distinct pattern of activation in feedback-associated layers during both the cue-induced suppression and subsequent attentional enhancement. These findings suggest that top-down modulation of V1 spiking can be bidirectional and result in either suppression or enhancement of spiking responses.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Attending to a visual stimulus increases its detectability, even if gaze is directed elsewhere. This covert attentional selection is known to enhance spiking across many brain areas, including the primary visual cortex (V1). Here we investigate the temporal dynamics of attention-related spiking changes in V1 of macaques performing a task that separates attentional selection from the onset of visual stimulation. We found that preceding attentional enhancement there was a sharp, transient decline in spiking following presentation of an attention-guiding cue. This disruption of V1 spiking was not observed in a task-naive subject that passively observed the same stimulus sequence, suggesting that sensory activation is insufficient to cause suppression. Following this suppression, attended stimuli evoked more spiking than unattended stimuli, matching previous reports of attention-related activity in V1. Laminar analyses revealed a distinct pattern of activation in feedback-associated layers during both the cue-induced suppression and subsequent attentional enhancement. These findings suggest that top-down modulation of V1 spiking can be bidirectional and result in either suppression or enhancement of spiking responses. |
Michele A Cox; Kacie Dougherty; Jacob A Westerberg; Michelle S Schall; Alexander Maier Temporal dynamics of binocular integration in primary visual cortex Journal Article Journal of Vision, 19 (12), pp. 1–21, 2019. @article{Cox2019b, title = {Temporal dynamics of binocular integration in primary visual cortex}, author = {Michele A Cox and Kacie Dougherty and Jacob A Westerberg and Michelle S Schall and Alexander Maier}, doi = {10.1167/19.12.13}, year = {2019}, date = {2019-01-01}, journal = {Journal of Vision}, volume = {19}, number = {12}, pages = {1--21}, abstract = {Whenever we open our eyes, our brain quickly integrates the two eyes' perspectives into a combined view. This process of binocular integration happens so rapidly that even incompatible stimuli are briefly fused before one eye's view is suppressed in favor of the other (binocular rivalry). The neuronal basis for this brief period of fusion during incompatible binocular stimulation is unclear. Neuroanatomically, the eyes provide two largely separate streams of information that are integrated into a binocular response by the primary visual cortex (V1). However, the temporal dynamics underlying the formation of this binocular response are largely unknown. To address this question, we examined the temporal profile of binocular responses in V1 of fixating monkeys. We found that V1 processes binocular stimuli in a dynamic sequence that comprises at least two distinct temporal phases. An initial transient phase is characterized by enhanced spiking responses for both compatible and incompatible binocular stimuli compared to monocular stimulation. This transient is followed by a sustained response that differed markedly between congruent and incongruent binocular stimulation. Specifically, incompatible binocular stimulation resulted in overall response reduction relative to monocular stimulation (binocular suppression). In contrast, responses to compatible stimuli were either suppressed or enhanced (binocular facilitation) depending on the neurons' ocularity (selectivity for one eye over the other) and laminar location. These results suggest that binocular integration in V1 occurs in at least two sequential steps that comprise initial additive combination of the two eyes' signals followed by widespread differentiation between binocular concordance and discordance.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Whenever we open our eyes, our brain quickly integrates the two eyes' perspectives into a combined view. This process of binocular integration happens so rapidly that even incompatible stimuli are briefly fused before one eye's view is suppressed in favor of the other (binocular rivalry). The neuronal basis for this brief period of fusion during incompatible binocular stimulation is unclear. Neuroanatomically, the eyes provide two largely separate streams of information that are integrated into a binocular response by the primary visual cortex (V1). However, the temporal dynamics underlying the formation of this binocular response are largely unknown. To address this question, we examined the temporal profile of binocular responses in V1 of fixating monkeys. We found that V1 processes binocular stimuli in a dynamic sequence that comprises at least two distinct temporal phases. An initial transient phase is characterized by enhanced spiking responses for both compatible and incompatible binocular stimuli compared to monocular stimulation. This transient is followed by a sustained response that differed markedly between congruent and incongruent binocular stimulation. Specifically, incompatible binocular stimulation resulted in overall response reduction relative to monocular stimulation (binocular suppression). In contrast, responses to compatible stimuli were either suppressed or enhanced (binocular facilitation) depending on the neurons' ocularity (selectivity for one eye over the other) and laminar location. These results suggest that binocular integration in V1 occurs in at least two sequential steps that comprise initial additive combination of the two eyes' signals followed by widespread differentiation between binocular concordance and discordance. |
Alexandre Dizeux; Marc Gesnik; Harry Ahnine; Kevin Blaize; Fabrice Arcizet; Serge Picaud; José Alain Sahel; Thomas Deffieux; Pierre Pouget; Mickael Tanter Functional ultrasound imaging of the brain reveals propagation of task-related brain activity in behaving primates Journal Article Nature Communications, 10 , pp. 1–9, 2019. @article{Dizeux2019, title = {Functional ultrasound imaging of the brain reveals propagation of task-related brain activity in behaving primates}, author = {Alexandre Dizeux and Marc Gesnik and Harry Ahnine and Kevin Blaize and Fabrice Arcizet and Serge Picaud and José Alain Sahel and Thomas Deffieux and Pierre Pouget and Mickael Tanter}, doi = {10.1038/s41467-019-09349-w}, year = {2019}, date = {2019-01-01}, journal = {Nature Communications}, volume = {10}, pages = {1--9}, abstract = {Neuroimaging modalities such as MRI and EEG are able to record from the whole brain, but this comes at the price of either limited spatiotemporal resolution or limited sensitivity. Here, we show that functional ultrasound imaging (fUS) of the brain is able to assess local changes in cerebral blood volume during cognitive tasks, with sufficient temporal resolution to measure the directional propagation of signals. In two macaques, we observed an abrupt transient change in supplementary eye field (SEF) activity when animals were required to modify their behaviour associated with a change of saccade tasks. SEF activation could be observed in a single trial, without averaging. Simultaneous imaging of anterior cingulate cortex and SEF revealed a time delay in the directional functional connectivity of 0.27 ± 0.07 s and 0.9 ± 0.2 s for both animals. Cerebral hemodynamics of large brain areas can be measured at high spatiotemporal resolution using fUS.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neuroimaging modalities such as MRI and EEG are able to record from the whole brain, but this comes at the price of either limited spatiotemporal resolution or limited sensitivity. Here, we show that functional ultrasound imaging (fUS) of the brain is able to assess local changes in cerebral blood volume during cognitive tasks, with sufficient temporal resolution to measure the directional propagation of signals. In two macaques, we observed an abrupt transient change in supplementary eye field (SEF) activity when animals were required to modify their behaviour associated with a change of saccade tasks. SEF activation could be observed in a single trial, without averaging. Simultaneous imaging of anterior cingulate cortex and SEF revealed a time delay in the directional functional connectivity of 0.27 ± 0.07 s and 0.9 ± 0.2 s for both animals. Cerebral hemodynamics of large brain areas can be measured at high spatiotemporal resolution using fUS. |
Lyndon Duong; Matthew Leavitt; Florian Pieper; Adam Sachs; Julio Martinez-Trujillo A normalization circuit underlying coding of spatial attention in primate lateral prefrontal cortex Journal Article eNeuro, 6 (2), pp. 1–23, 2019. @article{Duong2019, title = {A normalization circuit underlying coding of spatial attention in primate lateral prefrontal cortex}, author = {Lyndon Duong and Matthew Leavitt and Florian Pieper and Adam Sachs and Julio Martinez-Trujillo}, doi = {10.1523/ENEURO.0301-18.2019}, year = {2019}, date = {2019-01-01}, journal = {eNeuro}, volume = {6}, number = {2}, pages = {1--23}, abstract = {Lateral prefrontal cortex (LPFC) neurons signal the allocation of voluntary attention; however, the neural computations underlying this function remain unknown. To investigate this, we recorded from neuronal ensembles in the LPFC of two Macaca fascicularis performing a visuospatial attention task. LPFC neural responses to a single stimulus were normalized when additional stimuli/distracters appeared across the visual field and were wellcharacterized by an averaging computation. Deploying attention toward an individual stimulus surrounded by distracters shifted neural activity from an averaging regime toward a regime similar to that when the attended stimulus was presented in isolation (winner-take-all; WTA). However, attentional modulation is both qualitatively and quantitatively dependent on a neuron's visuospatial tuning. Our results show that during attentive vision, LPFC neuronal ensemble activity can be robustly read out by downstream areas to generate motor commands, and/or fed back into sensory areas to filter out distracter signals in favor of target signals.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Lateral prefrontal cortex (LPFC) neurons signal the allocation of voluntary attention; however, the neural computations underlying this function remain unknown. To investigate this, we recorded from neuronal ensembles in the LPFC of two Macaca fascicularis performing a visuospatial attention task. LPFC neural responses to a single stimulus were normalized when additional stimuli/distracters appeared across the visual field and were wellcharacterized by an averaging computation. Deploying attention toward an individual stimulus surrounded by distracters shifted neural activity from an averaging regime toward a regime similar to that when the attended stimulus was presented in isolation (winner-take-all; WTA). However, attentional modulation is both qualitatively and quantitatively dependent on a neuron's visuospatial tuning. Our results show that during attentive vision, LPFC neuronal ensemble activity can be robustly read out by downstream areas to generate motor commands, and/or fed back into sensory areas to filter out distracter signals in favor of target signals. |
Yang Fang; Ming Chen; Haoran Xu; Peichao Li; Chao Han; Jiaming Hu; Shude Zhu; Heng Ma; Haidong D Lu An orientation map for disparity-defined edges in area V4 Journal Article Cerebral Cortex, 29 (2), pp. 666–679, 2019. @article{Fang2019a, title = {An orientation map for disparity-defined edges in area V4}, author = {Yang Fang and Ming Chen and Haoran Xu and Peichao Li and Chao Han and Jiaming Hu and Shude Zhu and Heng Ma and Haidong D Lu}, doi = {10.1093/cercor/bhx348}, year = {2019}, date = {2019-01-01}, journal = {Cerebral Cortex}, volume = {29}, number = {2}, pages = {666--679}, abstract = {Binocular disparity information is an important source of 3D perception. Neurons sensitive to binocular disparity are found in almost all major visual areas in nonhuman primates. In area V4, disparity processes are suggested for the purposes of 3D-shape representation and fine disparity perception. However, whether neurons in V4 are sensitive to disparity-defined edges used in shape representation is not clear. Additionally, a functional organization for disparity edges has not been demonstrated so far. With intrinsic signal optical imaging, we studied functional organization for disparity edges in the monkey visual areas V1, V2, and V4. We found that there is an orientation map in V4 activated by edges purely defined by binocular disparity. This map is consistent with the orientation map obtained with regular luminance-defined edges, indicating a cue-invariant edge representation in this area. In contrast, such a map is much weaker in V2 and totally absent in V1. These findings reveal a hierarchical processing of 3D shape along the ventral pathway and the important role that V4 plays in shape-from-disparity detection.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Binocular disparity information is an important source of 3D perception. Neurons sensitive to binocular disparity are found in almost all major visual areas in nonhuman primates. In area V4, disparity processes are suggested for the purposes of 3D-shape representation and fine disparity perception. However, whether neurons in V4 are sensitive to disparity-defined edges used in shape representation is not clear. Additionally, a functional organization for disparity edges has not been demonstrated so far. With intrinsic signal optical imaging, we studied functional organization for disparity edges in the monkey visual areas V1, V2, and V4. We found that there is an orientation map in V4 activated by edges purely defined by binocular disparity. This map is consistent with the orientation map obtained with regular luminance-defined edges, indicating a cue-invariant edge representation in this area. In contrast, such a map is much weaker in V2 and totally absent in V1. These findings reveal a hierarchical processing of 3D shape along the ventral pathway and the important role that V4 plays in shape-from-disparity detection. |
Shiva Farashahi; Christopher H Donahue; Benjamin Y Hayden; Daeyeol Lee; Alireza Soltani Flexible combination of reward information across primates Journal Article Nature Human Behaviour, 3 (11), pp. 1215–1224, 2019. @article{Farashahi2019, title = {Flexible combination of reward information across primates}, author = {Shiva Farashahi and Christopher H Donahue and Benjamin Y Hayden and Daeyeol Lee and Alireza Soltani}, doi = {10.1038/s41562-019-0714-3}, year = {2019}, date = {2019-01-01}, journal = {Nature Human Behaviour}, volume = {3}, number = {11}, pages = {1215--1224}, publisher = {Springer US}, abstract = {A fundamental but rarely contested assumption in economics and neuroeconomics is that decision-makers compute subjective values of risky options by multiplying functions of reward probability and magnitude. By contrast, an additive strategy for valuation allows flexible combination of reward information required in uncertain or changing environments. We hypothesized that the level of uncertainty in the reward environment should determine the strategy used for valuation and choice. To test this hypothesis, we examined choice between risky options in humans and rhesus macaques across three tasks with different levels of uncertainty. We found that whereas humans and monkeys adopted a multiplicative strategy under risk when probabilities are known, both species spontaneously adopted an additive strategy under uncertainty when probabilities must be learned. Additionally, the level of volatility influenced relative weighting of certain and uncertain reward information, and this was reflected in the encoding of reward magnitude by neurons in the dorsolateral prefrontal cortex.}, keywords = {}, pubstate = {published}, tppubtype = {article} } A fundamental but rarely contested assumption in economics and neuroeconomics is that decision-makers compute subjective values of risky options by multiplying functions of reward probability and magnitude. By contrast, an additive strategy for valuation allows flexible combination of reward information required in uncertain or changing environments. We hypothesized that the level of uncertainty in the reward environment should determine the strategy used for valuation and choice. To test this hypothesis, we examined choice between risky options in humans and rhesus macaques across three tasks with different levels of uncertainty. We found that whereas humans and monkeys adopted a multiplicative strategy under risk when probabilities are known, both species spontaneously adopted an additive strategy under uncertainty when probabilities must be learned. Additionally, the level of volatility influenced relative weighting of certain and uncertain reward information, and this was reflected in the encoding of reward magnitude by neurons in the dorsolateral prefrontal cortex. |
Ian C Fiebelkorn; Mark A Pinsk; Sabine Kastner The mediodorsal pulvinar coordinates the macaque fronto-parietal network during rhythmic spatial attention Journal Article Nature Communications, 10 , pp. 1–15, 2019. @article{Fiebelkorn2019, title = {The mediodorsal pulvinar coordinates the macaque fronto-parietal network during rhythmic spatial attention}, author = {Ian C Fiebelkorn and Mark A Pinsk and Sabine Kastner}, doi = {10.1038/s41467-018-08151-4}, year = {2019}, date = {2019-01-01}, journal = {Nature Communications}, volume = {10}, pages = {1--15}, abstract = {Spatial attention is discontinuous, sampling behaviorally relevant locations in theta-rhythmic cycles (3-6 Hz). Underlying this rhythmic sampling are intrinsic theta oscillations in frontal and parietal cortices that provide a clocking mechanism for two alternating attentional states that are associated with either engagement at the presently attended location (and enhanced perceptual sensitivity) or disengagement (and diminished perceptual sensitivity). It has remained unclear, however, how these theta-dependent states are coordinated across the large-scale network that directs spatial attention. The pulvinar is a candidate for such coordination, having been previously shown to regulate cortical activity. Here, we examined pulvino-cortical interactions during theta-rhythmic sampling by simultaneously recording from macaque frontal eye fields (FEF), lateral intraparietal area (LIP), and pulvinar. Neural activity propagated from pulvinar to cortex during periods of engagement, and from cortex to pulvinar during periods of disengagement. A rhythmic reweighting of pulvino-cortical interactions thus defines functional dissociations in the attention network.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Spatial attention is discontinuous, sampling behaviorally relevant locations in theta-rhythmic cycles (3-6 Hz). Underlying this rhythmic sampling are intrinsic theta oscillations in frontal and parietal cortices that provide a clocking mechanism for two alternating attentional states that are associated with either engagement at the presently attended location (and enhanced perceptual sensitivity) or disengagement (and diminished perceptual sensitivity). It has remained unclear, however, how these theta-dependent states are coordinated across the large-scale network that directs spatial attention. The pulvinar is a candidate for such coordination, having been previously shown to regulate cortical activity. Here, we examined pulvino-cortical interactions during theta-rhythmic sampling by simultaneously recording from macaque frontal eye fields (FEF), lateral intraparietal area (LIP), and pulvinar. Neural activity propagated from pulvinar to cortex during periods of engagement, and from cortex to pulvinar during periods of disengagement. A rhythmic reweighting of pulvino-cortical interactions thus defines functional dissociations in the attention network. |
Nico A Flierman; Alla Ignashchenkova; Mario Negrello; Peter Thier; Chris I De Zeeuw; Aleksandra Badura Glissades are altered by lesions to the oculomotor vermis but not by saccadic adaptation Journal Article Frontiers in Behavioral Neuroscience, 13 , pp. 1–17, 2019. @article{Flierman2019, title = {Glissades are altered by lesions to the oculomotor vermis but not by saccadic adaptation}, author = {Nico A Flierman and Alla Ignashchenkova and Mario Negrello and Peter Thier and Chris I {De Zeeuw} and Aleksandra Badura}, doi = {10.3389/fnbeh.2019.00194}, year = {2019}, date = {2019-01-01}, journal = {Frontiers in Behavioral Neuroscience}, volume = {13}, pages = {1--17}, abstract = {Saccadic eye movements enable fast and precise scanning of the visual field, which is partially controlled by the posterior cerebellar vermis. Textbook saccades have a straight trajectory and a unimodal velocity profile, and hence have well-defined epochs of start and end. However, in practice only a fraction of saccades matches this description. One way in which a saccade can deviate from its trajectory is the presence of an overshoot or undershoot at the end of a saccadic eye movement just before fixation. This additional movement, known as a glissade, is regarded as a motor command error and was characterized decades ago but was almost never studied. Using rhesus macaques, we investigated the properties of glissades and changes to glissade kinematics following cerebellar lesions. Additionally, in monkeys with an intact cerebellum, we investigated whether the glissade amplitude can be modulated using multiple adaptation paradigms. Our results show that saccade kinematics are altered by the presence of a glissade, and that glissades do not appear to have any adaptive function as they do not bring the eye closer to the target. Quantification of these results establishes a detailed description of glissades. Further, we show that lesions to the posterior cerebellum have a deleterious effect on both saccade and glissade properties, which recovers over time. Finally, the saccadic adaptation experiments reveal that glissades cannot be modulated by this training paradigm. Together our work offers a functional study of glissades and provides new insight into the cerebellar involvement in this type of motor error.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Saccadic eye movements enable fast and precise scanning of the visual field, which is partially controlled by the posterior cerebellar vermis. Textbook saccades have a straight trajectory and a unimodal velocity profile, and hence have well-defined epochs of start and end. However, in practice only a fraction of saccades matches this description. One way in which a saccade can deviate from its trajectory is the presence of an overshoot or undershoot at the end of a saccadic eye movement just before fixation. This additional movement, known as a glissade, is regarded as a motor command error and was characterized decades ago but was almost never studied. Using rhesus macaques, we investigated the properties of glissades and changes to glissade kinematics following cerebellar lesions. Additionally, in monkeys with an intact cerebellum, we investigated whether the glissade amplitude can be modulated using multiple adaptation paradigms. Our results show that saccade kinematics are altered by the presence of a glissade, and that glissades do not appear to have any adaptive function as they do not bring the eye closer to the target. Quantification of these results establishes a detailed description of glissades. Further, we show that lesions to the posterior cerebellum have a deleterious effect on both saccade and glissade properties, which recovers over time. Finally, the saccadic adaptation experiments reveal that glissades cannot be modulated by this training paradigm. Together our work offers a functional study of glissades and provides new insight into the cerebellar involvement in this type of motor error. |
Maryam Ghahremani; Kevin D Johnston; Liya Ma; Lauren K Hayrynen; Stefan Everling Electrical microstimulation evokes saccades in posterior parietal cortex of common marmosets Journal Article Journal of Neurophysiology, 122 (4), pp. 1765–1776, 2019. @article{Ghahremani2019, title = {Electrical microstimulation evokes saccades in posterior parietal cortex of common marmosets}, author = {Maryam Ghahremani and Kevin D Johnston and Liya Ma and Lauren K Hayrynen and Stefan Everling}, doi = {10.1152/jn.00417.2019}, year = {2019}, date = {2019-01-01}, journal = {Journal of Neurophysiology}, volume = {122}, number = {4}, pages = {1765--1776}, abstract = {The common marmoset (Callithrix jacchus) is a small-bodied New World primate increasing in prominence as a model animal for neuroscience research. The lissencephalic cortex of this primate species provides substantial advantages for the application of electrophysiological techniques such as high-density and laminar recordings, which have the capacity to advance our understanding of local and laminar cortical circuits and their roles in cognitive and motor functions. This is particularly the case with respect to the oculomotor system, as critical cortical areas of this network such as the frontal eye fields (FEF) and lateral intraparietal area (LIP) lie deep within sulci in macaques. Studies of cytoarchitecture and connectivity have established putative homologies between cortical oculomotor fields in marmoset and macaque, but physiological investigations of these areas, particularly in awake marmosets, have yet to be carried out. Here we addressed this gap by probing the function of posterior parietal cortex of the common marmoset with electrical microstimulation. We implanted two animals with 32-channel Utah arrays at the location of the putative area LIP and applied microstimulation while they viewed a video display and made untrained eye movements. Similar to previous studies in macaques, stimulation evoked fixed-vector and goal-directed saccades, staircase saccades, and eyeblinks. These data demonstrate that area LIP of the marmoset plays a role in the regulation of eye movements, provide additional evidence that this area is homologous with that of the macaque, and further establish the marmoset as a valuable model for neurophysiological investigations of oculomotor and cognitive control.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The common marmoset (Callithrix jacchus) is a small-bodied New World primate increasing in prominence as a model animal for neuroscience research. The lissencephalic cortex of this primate species provides substantial advantages for the application of electrophysiological techniques such as high-density and laminar recordings, which have the capacity to advance our understanding of local and laminar cortical circuits and their roles in cognitive and motor functions. This is particularly the case with respect to the oculomotor system, as critical cortical areas of this network such as the frontal eye fields (FEF) and lateral intraparietal area (LIP) lie deep within sulci in macaques. Studies of cytoarchitecture and connectivity have established putative homologies between cortical oculomotor fields in marmoset and macaque, but physiological investigations of these areas, particularly in awake marmosets, have yet to be carried out. Here we addressed this gap by probing the function of posterior parietal cortex of the common marmoset with electrical microstimulation. We implanted two animals with 32-channel Utah arrays at the location of the putative area LIP and applied microstimulation while they viewed a video display and made untrained eye movements. Similar to previous studies in macaques, stimulation evoked fixed-vector and goal-directed saccades, staircase saccades, and eyeblinks. These data demonstrate that area LIP of the marmoset plays a role in the regulation of eye movements, provide additional evidence that this area is homologous with that of the macaque, and further establish the marmoset as a valuable model for neurophysiological investigations of oculomotor and cognitive control. |
Seyed Alireza Hassani; Sofia Lendor; Ezel Boyaci; Janusz Pawliszyn; Thilo Womelsdorf Multi-neuromodulator measurements across fronto-striatal network areas of the behaving macaque using solid-phase microextraction Journal Article Journal of Neurophysiology, 122 (4), pp. 1649–1660, 2019. @article{Hassani2019, title = {Multi-neuromodulator measurements across fronto-striatal network areas of the behaving macaque using solid-phase microextraction}, author = {Seyed Alireza Hassani and Sofia Lendor and Ezel Boyaci and Janusz Pawliszyn and Thilo Womelsdorf}, doi = {10.1152/jn.00321.2019}, year = {2019}, date = {2019-01-01}, journal = {Journal of Neurophysiology}, volume = {122}, number = {4}, pages = {1649--1660}, abstract = {Different neuromodulators rarely act independent from each other to modify neural processes but are instead coreleased, gated, or modulated. To understand this interdependence of neuromodulators and their collective influence on local circuits during different brain states, it is necessary to reliably extract local concentrations of multiple neuromodulators in vivo. Here we describe results using solid-phase microextraction (SPME), a method providing sensitive, multineuromodulator measurements. SPME is a sampling method that is coupled with mass spectrometry to quantify collected analytes. Reliable measurements of glutamate, dopamine, acetylcholine, and choline were made simultaneously within frontal cortex and striatum of two macaque monkeys (Macaca mulatta) during goal-directed behavior. We find glutamate concentrations several orders of magnitude higher than acetylcholine and dopamine in all brain regions. Dopamine was reliably detected in the striatum at tenfold higher concentrations than acetylcholine. Acetylcholine and choline concentrations were detected with high consistency across brain areas within monkeys and between monkeys. These findings illustrate that SPME microprobes provide a versatile novel tool to characterize multiple neuromodulators across different brain areas in vivo to understand the interdependence and covariation of neuromodulators during goal-directed behavior. Such data would be important to better distinguish between different behavioral states and characterize dysfunctional brain states that may be evident in psychiatric disorders.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Different neuromodulators rarely act independent from each other to modify neural processes but are instead coreleased, gated, or modulated. To understand this interdependence of neuromodulators and their collective influence on local circuits during different brain states, it is necessary to reliably extract local concentrations of multiple neuromodulators in vivo. Here we describe results using solid-phase microextraction (SPME), a method providing sensitive, multineuromodulator measurements. SPME is a sampling method that is coupled with mass spectrometry to quantify collected analytes. Reliable measurements of glutamate, dopamine, acetylcholine, and choline were made simultaneously within frontal cortex and striatum of two macaque monkeys (Macaca mulatta) during goal-directed behavior. We find glutamate concentrations several orders of magnitude higher than acetylcholine and dopamine in all brain regions. Dopamine was reliably detected in the striatum at tenfold higher concentrations than acetylcholine. Acetylcholine and choline concentrations were detected with high consistency across brain areas within monkeys and between monkeys. These findings illustrate that SPME microprobes provide a versatile novel tool to characterize multiple neuromodulators across different brain areas in vivo to understand the interdependence and covariation of neuromodulators during goal-directed behavior. Such data would be important to better distinguish between different behavioral states and characterize dysfunctional brain states that may be evident in psychiatric disorders. |
Shariq N Iqbal; Lun Yin; Caroline B Drucker; Qian Kuang; Jean-François Gariépy; Michael L Platt; John M Pearson Latent goal models for dynamic strategic interaction Journal Article PLoS Computational Biology, 15 (3), pp. 1–21, 2019. @article{Iqbal2019, title = {Latent goal models for dynamic strategic interaction}, author = {Shariq N Iqbal and Lun Yin and Caroline B Drucker and Qian Kuang and Jean-Fran{ç}ois Gariépy and Michael L Platt and John M Pearson}, doi = {10.1371/journal.pcbi.1006895}, year = {2019}, date = {2019-01-01}, journal = {PLoS Computational Biology}, volume = {15}, number = {3}, pages = {1--21}, abstract = {Understanding the principles by which agents interact with both complex environments and each other is a key goal of decision neuroscience. However, most previous studies have used experimental paradigms in which choices are discrete (and few), play is static, and optimal solutions are known. Yet in natural environments, interactions between agents typically involve continuous action spaces, ongoing dynamics, and no known optimal solution. Here, we seek to bridge this divide by using a "penalty shot" task in which pairs of monkeys competed against each other in a competitive, real-time video game. We modeled monkeys' strategies as driven by stochastically evolving goals, onscreen positions that served as set points for a control model that produced observed joystick movements. We fit this goal-based dynamical system model using approximate Bayesian inference methods, using neural networks to parameterize players' goals as a dynamic mixture of Gaussian components. Our model is conceptually simple, constructed of interpretable components, and capable of generating synthetic data that capture the complexity of real player dynamics. We further characterized players' strategies using the number of change points on each trial. We found that this complexity varied more across sessions than within sessions, and that more complex strategies benefited offensive players but not defensive players. Together, our experimental paradigm and model offer a powerful combination of tools for the study of realistic social dynamics in the laboratory setting.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Understanding the principles by which agents interact with both complex environments and each other is a key goal of decision neuroscience. However, most previous studies have used experimental paradigms in which choices are discrete (and few), play is static, and optimal solutions are known. Yet in natural environments, interactions between agents typically involve continuous action spaces, ongoing dynamics, and no known optimal solution. Here, we seek to bridge this divide by using a "penalty shot" task in which pairs of monkeys competed against each other in a competitive, real-time video game. We modeled monkeys' strategies as driven by stochastically evolving goals, onscreen positions that served as set points for a control model that produced observed joystick movements. We fit this goal-based dynamical system model using approximate Bayesian inference methods, using neural networks to parameterize players' goals as a dynamic mixture of Gaussian components. Our model is conceptually simple, constructed of interpretable components, and capable of generating synthetic data that capture the complexity of real player dynamics. We further characterized players' strategies using the number of change points on each trial. We found that this complexity varied more across sessions than within sessions, and that more complex strategies benefited offensive players but not defensive players. Together, our experimental paradigm and model offer a powerful combination of tools for the study of realistic social dynamics in the laboratory setting. |
Anna Ivic Jasper; Seiji Tanabe; Adam Kohn Predicting perceptual decisions using visual cortical population responses and choice history Journal Article The Journal of Neuroscience, 39 (34), pp. 6714–6727, 2019. @article{Jasper2019, title = {Predicting perceptual decisions using visual cortical population responses and choice history}, author = {Anna Ivic Jasper and Seiji Tanabe and Adam Kohn}, year = {2019}, date = {2019-01-01}, journal = {The Journal of Neuroscience}, volume = {39}, number = {34}, pages = {6714--6727}, abstract = {Our understanding ofthe neural basis ofperceptual decision making has been built in part on relating co-fluctuations ofsingle neuron responses to perceptual decisions on a trial-by-trial basis. The strength of this relationship is often compared across neurons or brain areas, recorded in different sessions, animals, or variants ofa task.Wesought to extend our understanding ofperceptual decision making in three ways. First, we measured neuronal activity simultaneously in early [primary visual cortex ( V1)] and midlevel (V4) visual cortex while macaque monkeys performed a fine orientation discrimination perceptual task. This allowed a direct comparison ofchoice signals in these two areas, including their dynamics. Second, we asked how our ability to predict animals' decisions would be improved by considering small simultaneously-recorded neuronal populations rather than individual units. Finally, we asked whether predictions would be improved by taking into account the animals' choice and reward histories, which can strongly influence decision making. We found that responses ofindividual V4 neurons were weakly predictive ofdecisions, but only in a briefepoch between stimulus offset and the indication of choice. In V1, few neurons showed significant decision-related activity. Analysis of neuronal population responses revealed robust choice-related information in V4 and substantially weaker signals in V1. Including choice- and reward-history informa- tion improved performance further, particularly when the recorded populations contained little decision-related information. Our work shows the power ofusing neuronal populations and decision history when relating neuronal responses to the perceptual decisions they are thought to underlie.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Our understanding ofthe neural basis ofperceptual decision making has been built in part on relating co-fluctuations ofsingle neuron responses to perceptual decisions on a trial-by-trial basis. The strength of this relationship is often compared across neurons or brain areas, recorded in different sessions, animals, or variants ofa task.Wesought to extend our understanding ofperceptual decision making in three ways. First, we measured neuronal activity simultaneously in early [primary visual cortex ( V1)] and midlevel (V4) visual cortex while macaque monkeys performed a fine orientation discrimination perceptual task. This allowed a direct comparison ofchoice signals in these two areas, including their dynamics. Second, we asked how our ability to predict animals' decisions would be improved by considering small simultaneously-recorded neuronal populations rather than individual units. Finally, we asked whether predictions would be improved by taking into account the animals' choice and reward histories, which can strongly influence decision making. We found that responses ofindividual V4 neurons were weakly predictive ofdecisions, but only in a briefepoch between stimulus offset and the indication of choice. In V1, few neurons showed significant decision-related activity. Analysis of neuronal population responses revealed robust choice-related information in V4 and substantially weaker signals in V1. Including choice- and reward-history informa- tion improved performance further, particularly when the recorded populations contained little decision-related information. Our work shows the power ofusing neuronal populations and decision history when relating neuronal responses to the perceptual decisions they are thought to underlie. |
Kevin Johnston; Liya Ma; Lauren Schaeffer Alpha oscillations modulate preparatory activity in marmoset area 8Ad Journal Article The Journal of Neuroscience, 39 (10), pp. 855–1866, 2019. @article{Johnston2019, title = {Alpha oscillations modulate preparatory activity in marmoset area 8Ad}, author = {Kevin Johnston and Liya Ma and Lauren Schaeffer}, doi = {10.1523/JNEUROSCI.2703-18.2019}, year = {2019}, date = {2019-01-01}, journal = {The Journal of Neuroscience}, volume = {39}, number = {10}, pages = {855--1866}, abstract = {Cognitive control often requires suppression of prepotent stimulus-driven responses in favor of less potent alternatives. Suppression of prepotent saccades has been shown to require proactive inhibition in the frontoparietal saccade network. Electrophysiological evidence in macaque monkeys has revealed neural correlates of such inhibition in this network; however, the interlaminar instantiation of inhibitory processes remains poorly understood because these areas lie deep within sulci in macaques, rendering them inaccessible to laminar recordings. Here, we addressed this gap by exploiting the mostly lissencephalic cortex of the common marmoset (Callithrix jacchus). We inserted linear electrode arrays into areas 8Ad-the putative marmoset frontal eye field-and the lateral intraparietal area of two male marmosets and recorded neural activity during performance of a task comprised of alternating blocks of trials requiring a saccade either toward a large, high-luminance stimulus or the inhibition of this prepotent response in favor of a saccade toward a small, low-luminance stimulus. We observed prominent task-dependent activity in both alpha/gamma bands of the LFP and discharge rates of single neurons in area 8Ad during a prestimulus task epoch in which the animals had been instructed which of these two tasks to perform but before peripheral stimulus onset. These data are consistent with a model in which rhythmic alpha-band activity in deeper layers inhibits spiking in upper layers to support proactive inhibitory saccade control.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Cognitive control often requires suppression of prepotent stimulus-driven responses in favor of less potent alternatives. Suppression of prepotent saccades has been shown to require proactive inhibition in the frontoparietal saccade network. Electrophysiological evidence in macaque monkeys has revealed neural correlates of such inhibition in this network; however, the interlaminar instantiation of inhibitory processes remains poorly understood because these areas lie deep within sulci in macaques, rendering them inaccessible to laminar recordings. Here, we addressed this gap by exploiting the mostly lissencephalic cortex of the common marmoset (Callithrix jacchus). We inserted linear electrode arrays into areas 8Ad-the putative marmoset frontal eye field-and the lateral intraparietal area of two male marmosets and recorded neural activity during performance of a task comprised of alternating blocks of trials requiring a saccade either toward a large, high-luminance stimulus or the inhibition of this prepotent response in favor of a saccade toward a small, low-luminance stimulus. We observed prominent task-dependent activity in both alpha/gamma bands of the LFP and discharge rates of single neurons in area 8Ad during a prestimulus task epoch in which the animals had been instructed which of these two tasks to perform but before peripheral stimulus onset. These data are consistent with a model in which rhythmic alpha-band activity in deeper layers inhibits spiking in upper layers to support proactive inhibitory saccade control. |
Kohitij Kar; Jonas Kubilius; Kailyn Schmidt; Elias B Issa; James J DiCarlo Evidence that recurrent circuits are critical to the ventral stream's execution of core object recognition behavior Journal Article Nature Neuroscience, 22 , pp. 974–983, 2019. @article{Kar2019, title = {Evidence that recurrent circuits are critical to the ventral stream's execution of core object recognition behavior}, author = {Kohitij Kar and Jonas Kubilius and Kailyn Schmidt and Elias B Issa and James J DiCarlo}, doi = {10.1038/s41593-019-0392-5}, year = {2019}, date = {2019-01-01}, journal = {Nature Neuroscience}, volume = {22}, pages = {974--983}, abstract = {Non-recurrent deep convolutional neural networks (CNNs) are currently the best at modeling core object recognition, a behavior that is supported by the densely recurrent primate ventral stream, culminating in the inferior temporal (IT) cortex. If recurrence is critical to this behavior, then primates should outperform feedforward-only deep CNNs for images that require additional recurrent processing beyond the feedforward IT response. Here we first used behavioral methods to discover hundreds of these ‘challenge' images. Second, using large-scale electrophysiology, we observed that behaviorally sufficient object identity solutions emerged ~30 ms later in the IT cortex for challenge images compared with primate performance-matched ‘control' images. Third, these behaviorally critical late-phase IT response patterns were poorly predicted by feedforward deep CNN activations. Notably, very-deep CNNs and shallower recurrent CNNs better predicted these late IT responses, suggesting that there is a functional equivalence between additional nonlinear transformations and recurrence. Beyond arguing that recurrent circuits are critical for rapid object identification, our results provide strong constraints for future recurrent model development.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Non-recurrent deep convolutional neural networks (CNNs) are currently the best at modeling core object recognition, a behavior that is supported by the densely recurrent primate ventral stream, culminating in the inferior temporal (IT) cortex. If recurrence is critical to this behavior, then primates should outperform feedforward-only deep CNNs for images that require additional recurrent processing beyond the feedforward IT response. Here we first used behavioral methods to discover hundreds of these ‘challenge' images. Second, using large-scale electrophysiology, we observed that behaviorally sufficient object identity solutions emerged ~30 ms later in the IT cortex for challenge images compared with primate performance-matched ‘control' images. Third, these behaviorally critical late-phase IT response patterns were poorly predicted by feedforward deep CNN activations. Notably, very-deep CNNs and shallower recurrent CNNs better predicted these late IT responses, suggesting that there is a functional equivalence between additional nonlinear transformations and recurrence. Beyond arguing that recurrent circuits are critical for rapid object identification, our results provide strong constraints for future recurrent model development. |
Sanjeev B Khanna; Adam C Snyder; Matthew A Smith Distinct sources of variability affect eye movement preparation Journal Article The Journal of Neuroscience, 39 (23), pp. 4511–4526, 2019. @article{Khanna2019, title = {Distinct sources of variability affect eye movement preparation}, author = {Sanjeev B Khanna and Adam C Snyder and Matthew A Smith}, doi = {10.1523/JNEUROSCI.2329-18.2019}, year = {2019}, date = {2019-01-01}, journal = {The Journal of Neuroscience}, volume = {39}, number = {23}, pages = {4511--4526}, abstract = {The sequence of events leading to an eye movement to a target begins the moment visual information has reached the brain, well in advance of the eye movement itself. The process by which visual information is encoded and used to generate a motor plan has been the focus of substantial interest partly because of the rapid and reproducible nature of saccadic eye movements, and the key role that they play in primate behavior. Signals related to eye movements are present in much of the primate brain, yet most neurophysiological studies of the transition from vision to eye movements have measured the activity of one neuron at a time. Less is known about how the coordinated action of populations of neurons contribute to the initiation of eye movements. One cortical area of particular interest in this process is the frontal eye fields, a region of prefrontal cortex that has descending projections to oculomotor control centers. We recorded from populations of frontal eye field neurons in macaque monkeys engaged in a memory-guided saccade task. We found a variety of neurons with visually evoked responses, saccade-aligned responses, and mixtures of both. We took advantage of the simultaneous nature of the recordings to measure variability in individual neurons and pairs of neurons from trial-to-trial, as well as the moment-to-moment population activity structure.Wefound that these measures were related to saccadic reaction times, suggesting that the population-level organization of frontal eye field activity is important for the transition from perception to movement.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The sequence of events leading to an eye movement to a target begins the moment visual information has reached the brain, well in advance of the eye movement itself. The process by which visual information is encoded and used to generate a motor plan has been the focus of substantial interest partly because of the rapid and reproducible nature of saccadic eye movements, and the key role that they play in primate behavior. Signals related to eye movements are present in much of the primate brain, yet most neurophysiological studies of the transition from vision to eye movements have measured the activity of one neuron at a time. Less is known about how the coordinated action of populations of neurons contribute to the initiation of eye movements. One cortical area of particular interest in this process is the frontal eye fields, a region of prefrontal cortex that has descending projections to oculomotor control centers. We recorded from populations of frontal eye field neurons in macaque monkeys engaged in a memory-guided saccade task. We found a variety of neurons with visually evoked responses, saccade-aligned responses, and mixtures of both. We took advantage of the simultaneous nature of the recordings to measure variability in individual neurons and pairs of neurons from trial-to-trial, as well as the moment-to-moment population activity structure.Wefound that these measures were related to saccadic reaction times, suggesting that the population-level organization of frontal eye field activity is important for the transition from perception to movement. |
Seolmin Kim; Jeongjun Park; Joonyeol Lee Effect of prior direction expectation on the accuracy and precision of smooth pursuit eye movements Journal Article Frontiers in Systems Neuroscience, 13 , pp. 1–12, 2019. @article{Kim2019d, title = {Effect of prior direction expectation on the accuracy and precision of smooth pursuit eye movements}, author = {Seolmin Kim and Jeongjun Park and Joonyeol Lee}, doi = {10.3389/fnsys.2019.00071}, year = {2019}, date = {2019-01-01}, journal = {Frontiers in Systems Neuroscience}, volume = {13}, pages = {1--12}, abstract = {The integration of sensory with top–down cognitive signals for generating appropriate sensory–motor behaviors is an important issue in understanding the brain's information processes. Recent studies have demonstrated that the interplay between sensory and high-level signals in oculomotor behavior could be explained by Bayesian inference. Specifically, prior knowledge for motion speed introduces a bias in the speed of smooth pursuit eye movements. The other important prediction of Bayesian inference is variability reduction by prior expectation; however, there is insufficient evidence in oculomotor behaviors to support this prediction. In the present study, we trained monkeys to switch the prior expectation about motion direction and independently controlled the strength of the motion stimulus. Under identical sensory stimulus conditions, we tested if prior knowledge about the motion direction reduced the variability of open-loop smooth pursuit eye movements. We observed a significant reduction when the prior expectation was strong; this was consistent with the prediction of Bayesian inference. Taking advantage of the open-loop smooth pursuit, we investigated the temporal dynamics of the effect of the prior to the pursuit direction bias and variability. This analysis demonstrated that the strength of the sensory evidence depended not only on the strength of the sensory stimulus but also on the time required for the pursuit system to form a neural sensory representation. Finally, we demonstrated that the variability and directional bias change by prior knowledge were quantitatively explained by the Bayesian observer model.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The integration of sensory with top–down cognitive signals for generating appropriate sensory–motor behaviors is an important issue in understanding the brain's information processes. Recent studies have demonstrated that the interplay between sensory and high-level signals in oculomotor behavior could be explained by Bayesian inference. Specifically, prior knowledge for motion speed introduces a bias in the speed of smooth pursuit eye movements. The other important prediction of Bayesian inference is variability reduction by prior expectation; however, there is insufficient evidence in oculomotor behaviors to support this prediction. In the present study, we trained monkeys to switch the prior expectation about motion direction and independently controlled the strength of the motion stimulus. Under identical sensory stimulus conditions, we tested if prior knowledge about the motion direction reduced the variability of open-loop smooth pursuit eye movements. We observed a significant reduction when the prior expectation was strong; this was consistent with the prediction of Bayesian inference. Taking advantage of the open-loop smooth pursuit, we investigated the temporal dynamics of the effect of the prior to the pursuit direction bias and variability. This analysis demonstrated that the strength of the sensory evidence depended not only on the strength of the sensory stimulus but also on the time required for the pursuit system to form a neural sensory representation. Finally, we demonstrated that the variability and directional bias change by prior knowledge were quantitatively explained by the Bayesian observer model. |
Taekjun Kim; Wyeth Bair; Anitha Pasupathy Neural coding for shape and texture in macaque area V4 Journal Article The Journal of Neuroscience, 39 (24), pp. 4760–4774, 2019. @article{Kim2019e, title = {Neural coding for shape and texture in macaque area V4}, author = {Taekjun Kim and Wyeth Bair and Anitha Pasupathy}, doi = {10.1523/JNEUROSCI.3073-18.2019}, year = {2019}, date = {2019-01-01}, journal = {The Journal of Neuroscience}, volume = {39}, number = {24}, pages = {4760--4774}, abstract = {The distinct visual sensations of shape and texture have been studied separately in cortex; therefore, it remains unknown whether separate neuronal populations encode each of these properties or one population carries a joint encoding. We directly compared shape and texture selectivity of individual V4 neurons in awake macaques (1 male, 1 female) and found that V4 neurons lie along a continuum from strong tuning for boundary curvature of shapes to strong tuning for perceptual dimensions of texture. Among neurons tuned to both attributes, tuning for shape and texture were largely separable, with the latter delayed by ~30 ms. We also found that shape stimuli typically evoked stronger, more selective responses than did texture patches, regardless of whether the latter were contained within or extended beyond the receptive field. These results suggest that there are separate specializations in mid-level cortical processing for visual attributes of shape and texture.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The distinct visual sensations of shape and texture have been studied separately in cortex; therefore, it remains unknown whether separate neuronal populations encode each of these properties or one population carries a joint encoding. We directly compared shape and texture selectivity of individual V4 neurons in awake macaques (1 male, 1 female) and found that V4 neurons lie along a continuum from strong tuning for boundary curvature of shapes to strong tuning for perceptual dimensions of texture. Among neurons tuned to both attributes, tuning for shape and texture were largely separable, with the latter delayed by ~30 ms. We also found that shape stimuli typically evoked stronger, more selective responses than did texture patches, regardless of whether the latter were contained within or extended beyond the receptive field. These results suggest that there are separate specializations in mid-level cortical processing for visual attributes of shape and texture. |
Satwant Kumar; Ivo D Popivanov; Rufin Vogels Transformation of visual representations across ventral stream body-selective patches Journal Article Cerebral Cortex, 29 , pp. 215–229, 2019. @article{Kumar2019a, title = {Transformation of visual representations across ventral stream body-selective patches}, author = {Satwant Kumar and Ivo D Popivanov and Rufin Vogels}, doi = {10.1093/cercor/bhx320}, year = {2019}, date = {2019-01-01}, journal = {Cerebral Cortex}, volume = {29}, pages = {215--229}, abstract = {Although the neural processing of visual images of bodies is critical for survival, it is much less well understood than face processing. Functional imaging studies demonstrated body selective regions in primate inferior temporal cortex. To advance our understanding of how the visual brain represents bodies, we compared the representation of animate and inanimate objects in two such body patches with fMRI-guided single unit recordings in rhesus monkeys. We found that the middle Superior Temporal Sulcus body patch (MSB) distinguishes to a greater extent bodies from non-bodies than the anterior Superior Temporal Sulcus body patch (ASB). Importantly, ASB carried more viewpoint-tolerant information about body posture and body identity than MSB, while MSB showed greater orientation selectivity. Combined with previous work on faces, this suggests that an increase in view-tolerant representations, coupled with a refined individuation, along the visual hierarchy is a general property of information processing within the inferior temporal cortex.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Although the neural processing of visual images of bodies is critical for survival, it is much less well understood than face processing. Functional imaging studies demonstrated body selective regions in primate inferior temporal cortex. To advance our understanding of how the visual brain represents bodies, we compared the representation of animate and inanimate objects in two such body patches with fMRI-guided single unit recordings in rhesus monkeys. We found that the middle Superior Temporal Sulcus body patch (MSB) distinguishes to a greater extent bodies from non-bodies than the anterior Superior Temporal Sulcus body patch (ASB). Importantly, ASB carried more viewpoint-tolerant information about body posture and body identity than MSB, while MSB showed greater orientation selectivity. Combined with previous work on faces, this suggests that an increase in view-tolerant representations, coupled with a refined individuation, along the visual hierarchy is a general property of information processing within the inferior temporal cortex. |
Satwant Kumar; Rufin Vogels Body patches in inferior temporal cortex encode categories with different temporal dynamics Journal Article Journal of Cognitive Neuroscience, 31 (11), pp. 1699–1709, 2019. @article{Kumar2019b, title = {Body patches in inferior temporal cortex encode categories with different temporal dynamics}, author = {Satwant Kumar and Rufin Vogels}, doi = {10.1162/jocn}, year = {2019}, date = {2019-01-01}, journal = {Journal of Cognitive Neuroscience}, volume = {31}, number = {11}, pages = {1699--1709}, abstract = {An unresolved question in cognitive neuroscience is how representations of object categories at different levels (basic and superordinate) develop during the course of the neural response within an area. To address this, we decoded categories of different levels from the spiking responses of populations of neurons recorded in two fMRI-defined body patches in the macaque STS. Recordings of the two patches were made in thesameanimals with thesamestimuli. Support vector machine classifiers were trained at brief response epochs and tested at the same or different epochs, thus assessing whether category representations change during the course of the response. In agreement with hierarchical processing within the body patch network, the posterior body patch mid STS body (MSB) showed an earlier onset of categorization compared with the anterior body patch anterior STS body (ASB), irrespective of the categorization level. Decoding of the superordinate body versus nonbody categories was less dynamic in MSB than in ASB, with ASB showing a biphasic temporal pattern. Decoding of the ordinate-level category human versus monkey bodies showed similar temporal patterns in both patches. The decoding onset of superordinate categorizations involving bodies was as early as for basic-level categorization, suggesting that previously reported differences between the onset of basic and superordinate categorizations may depend on the area. The qualitative difference between areas in their dynamics of category representation may hinder the interpretation of decoding dynamics based on EEG or MEG, methods that may mix signals of different areas.}, keywords = {}, pubstate = {published}, tppubtype = {article} } An unresolved question in cognitive neuroscience is how representations of object categories at different levels (basic and superordinate) develop during the course of the neural response within an area. To address this, we decoded categories of different levels from the spiking responses of populations of neurons recorded in two fMRI-defined body patches in the macaque STS. Recordings of the two patches were made in thesameanimals with thesamestimuli. Support vector machine classifiers were trained at brief response epochs and tested at the same or different epochs, thus assessing whether category representations change during the course of the response. In agreement with hierarchical processing within the body patch network, the posterior body patch mid STS body (MSB) showed an earlier onset of categorization compared with the anterior body patch anterior STS body (ASB), irrespective of the categorization level. Decoding of the superordinate body versus nonbody categories was less dynamic in MSB than in ASB, with ASB showing a biphasic temporal pattern. Decoding of the ordinate-level category human versus monkey bodies showed similar temporal patterns in both patches. The decoding onset of superordinate categorizations involving bodies was as early as for basic-level categorization, suggesting that previously reported differences between the onset of basic and superordinate categorizations may depend on the area. The qualitative difference between areas in their dynamics of category representation may hinder the interpretation of decoding dynamics based on EEG or MEG, methods that may mix signals of different areas. |
Noga Larry; Merav Yarkoni; Adi Lixenberg; Mati Joshua Cerebellar climbing fibers encode expected reward size Journal Article eLife, 8 , pp. 1–16, 2019. @article{Larry2019, title = {Cerebellar climbing fibers encode expected reward size}, author = {Noga Larry and Merav Yarkoni and Adi Lixenberg and Mati Joshua}, doi = {10.7554/eLife.46870}, year = {2019}, date = {2019-01-01}, journal = {eLife}, volume = {8}, pages = {1--16}, abstract = {Climbing fiber inputs to the cerebellum encode error signals that instruct learning. Recently, evidence has accumulated to suggest that the cerebellum is also involved in the processing of reward. To study how rewarding events are encoded, we recorded the activity of climbing fibers when monkeys were engaged in an eye movement task. At the beginning of each trial, the monkeys were cued to the size of the reward that would be delivered upon successful completion of the trial. Climbing fiber activity increased when the monkeys were presented with a cue indicating a large reward size. Reward size did not modulate activity at reward delivery or during eye movements. Comparison between climbing fiber and simple spike activity indicated different interactions for coding of movement and reward. These results indicate that climbing fibers encode the expected reward size and suggest a general role of the cerebellum in associative learning beyond error correction.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Climbing fiber inputs to the cerebellum encode error signals that instruct learning. Recently, evidence has accumulated to suggest that the cerebellum is also involved in the processing of reward. To study how rewarding events are encoded, we recorded the activity of climbing fibers when monkeys were engaged in an eye movement task. At the beginning of each trial, the monkeys were cued to the size of the reward that would be delivered upon successful completion of the trial. Climbing fiber activity increased when the monkeys were presented with a cue indicating a large reward size. Reward size did not modulate activity at reward delivery or during eye movements. Comparison between climbing fiber and simple spike activity indicated different interactions for coding of movement and reward. These results indicate that climbing fibers encode the expected reward size and suggest a general role of the cerebellum in associative learning beyond error correction. |
Yin S Li; Matthew R Nassar; Joseph W Kable; Joshua I Gold Individual neurons in the cingulate cortex encode action monitoring, not selection, during adaptive decision-making Journal Article The Journal of Neuroscience, 39 (34), pp. 6668–6683, 2019. @article{Li2019g, title = {Individual neurons in the cingulate cortex encode action monitoring, not selection, during adaptive decision-making}, author = {Yin S Li and Matthew R Nassar and Joseph W Kable and Joshua I Gold}, doi = {10.1523/JNEUROSCI.0159-19.2019}, year = {2019}, date = {2019-01-01}, journal = {The Journal of Neuroscience}, volume = {39}, number = {34}, pages = {6668--6683}, abstract = {The cingulate cortex contributes to complex, adaptive behaviors, but the exact nature of its contributions remains unresolved. Proposals from previous studies, including evaluating past actions or selecting future ones, have been difficult to distinguish in part because of an incomplete understanding of the task-relevant variables that are encoded by individual cingulate neurons. In this study, we recorded from individual neurons in parts ofboth the anterior cingulate cortex (ACC) and posterior cingulate cortex (PCC) in 2 male rhesus monkeys performing a saccadic reward task. The task required them to use adaptive, feedback-driven strategies to infer the spatial location ofa rewarded saccade target in the presence ofdifferent forms ofuncertainty. We found that task-relevant, spatially selective feedback signals were encoded by the activity of individual neurons in both brain regions, with stronger selectivity for spatial choice and reward-target signals in PCC and stronger selectivity for feedback in ACC. Moreover, neurons in both regions were sensitive to sequential effects of feedback that partly reflected sequential behavioral patterns. However, neither brain region exhibited systematic modulations by the blockwise conditions that governed the reliability of the trial-by-trial feedback and drove adaptive behavioral patterns. There was also little evidence that single-neuron responses in either brain region directly predicted the extent to which feedback and contextual information were used to inform choices on the subsequent trial. Thus, certain cingulate neurons encode diverse, evaluative signals needed for adaptive, feedback-driven decision-making, but those signals may be integrated elsewhere in the brain to guide actions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The cingulate cortex contributes to complex, adaptive behaviors, but the exact nature of its contributions remains unresolved. Proposals from previous studies, including evaluating past actions or selecting future ones, have been difficult to distinguish in part because of an incomplete understanding of the task-relevant variables that are encoded by individual cingulate neurons. In this study, we recorded from individual neurons in parts ofboth the anterior cingulate cortex (ACC) and posterior cingulate cortex (PCC) in 2 male rhesus monkeys performing a saccadic reward task. The task required them to use adaptive, feedback-driven strategies to infer the spatial location ofa rewarded saccade target in the presence ofdifferent forms ofuncertainty. We found that task-relevant, spatially selective feedback signals were encoded by the activity of individual neurons in both brain regions, with stronger selectivity for spatial choice and reward-target signals in PCC and stronger selectivity for feedback in ACC. Moreover, neurons in both regions were sensitive to sequential effects of feedback that partly reflected sequential behavioral patterns. However, neither brain region exhibited systematic modulations by the blockwise conditions that governed the reliability of the trial-by-trial feedback and drove adaptive behavioral patterns. There was also little evidence that single-neuron responses in either brain region directly predicted the extent to which feedback and contextual information were used to inform choices on the subsequent trial. Thus, certain cingulate neurons encode diverse, evaluative signals needed for adaptive, feedback-driven decision-making, but those signals may be integrated elsewhere in the brain to guide actions. |
Junxiang Luo; Keyan He; Ian Max Andolina; Xiaohong Li; Jiapeng Yin; Zheyuan Chen; Yong Gu; Wei Wang Going with the flow: The neural mechanisms underlying illusions of complex-flow motion Journal Article The Journal of Neuroscience, 39 (14), pp. 2664 –2685, 2019. @article{Luo2019, title = {Going with the flow: The neural mechanisms underlying illusions of complex-flow motion}, author = {Junxiang Luo and Keyan He and Ian Max Andolina and Xiaohong Li and Jiapeng Yin and Zheyuan Chen and Yong Gu and Wei Wang}, doi = {10.1523/JNEUROSCI.2112-18.2019}, year = {2019}, date = {2019-01-01}, journal = {The Journal of Neuroscience}, volume = {39}, number = {14}, pages = {2664 --2685}, abstract = {Studying the mismatch between perception and reality helps us better understand the constructive nature of the visual brain. The Pinna-Brelstaff motion illusion is a compelling example illustrating how a complex moving pattern can generate an illusory motion perception. When an observer moves toward (expansion) or away (contraction) from the Pinna-Brelstaff figure, the figure appears to rotate. The neural mechanisms underlying the illusory complex-flow motion of rotation, expansion, and contraction remain unknown. We studied this question at both perceptual and neuronal levels in behaving male macaques by using carefully parametrized Pinna-Brelstaff figures that induce the above motion illusions. We first demonstrate that macaques perceive illusory motion in a manner similar to that of human observers. Neurophysiological recordings were subsequently performed in the middle temporal area (MT) and the dorsal portion of the medial superior temporal area (MSTd). We find that subgroups of MSTd neurons encoding a particular global pattern of real complex-flow motion (rotation, expansion, contraction) also represent illusory motion patterns of the same class. They require an extra 15 ms to reliably discriminate the illusion. In contrast, MT neurons encode both real and illusory local motions with similar temporal delays. These findings reveal that illusory complex-flow motion is first represented in MSTd by the same neurons that normally encode real complex-flow motion. However, the extraction of global illusory motion in MSTd from other classes of real complex-flow motion requires extra processing time. Our study illustrates a cascaded integration mechanism from MT to MSTd underlying the transformation from external physical to internal nonveridical flow-motion perception.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Studying the mismatch between perception and reality helps us better understand the constructive nature of the visual brain. The Pinna-Brelstaff motion illusion is a compelling example illustrating how a complex moving pattern can generate an illusory motion perception. When an observer moves toward (expansion) or away (contraction) from the Pinna-Brelstaff figure, the figure appears to rotate. The neural mechanisms underlying the illusory complex-flow motion of rotation, expansion, and contraction remain unknown. We studied this question at both perceptual and neuronal levels in behaving male macaques by using carefully parametrized Pinna-Brelstaff figures that induce the above motion illusions. We first demonstrate that macaques perceive illusory motion in a manner similar to that of human observers. Neurophysiological recordings were subsequently performed in the middle temporal area (MT) and the dorsal portion of the medial superior temporal area (MSTd). We find that subgroups of MSTd neurons encoding a particular global pattern of real complex-flow motion (rotation, expansion, contraction) also represent illusory motion patterns of the same class. They require an extra 15 ms to reliably discriminate the illusion. In contrast, MT neurons encode both real and illusory local motions with similar temporal delays. These findings reveal that illusory complex-flow motion is first represented in MSTd by the same neurons that normally encode real complex-flow motion. However, the extraction of global illusory motion in MSTd from other classes of real complex-flow motion requires extra processing time. Our study illustrates a cascaded integration mechanism from MT to MSTd underlying the transformation from external physical to internal nonveridical flow-motion perception. |
Liya Ma; Jason L Chan; Kevin Johnston; Stephen G Lomber; Stefan Everling Macaque anterior cingulate cortex deactivation impairs performance and alters lateral prefrontal oscillatory activities in a rule-switching task Journal Article 17 (7), pp. 1–37, 2019. @article{Ma2019b, title = {Macaque anterior cingulate cortex deactivation impairs performance and alters lateral prefrontal oscillatory activities in a rule-switching task}, author = {Liya Ma and Jason L Chan and Kevin Johnston and Stephen G Lomber and Stefan Everling}, doi = {10.1371/journal.pbio.3000045}, year = {2019}, date = {2019-01-01}, booktitle = {PLoS Biology}, volume = {17}, number = {7}, pages = {1--37}, abstract = {In primates, both the dorsal anterior cingulate cortex (dACC) and the dorsolateral prefrontal cortex (dlPFC) are key regions of the frontoparietal cognitive control network. To study the role of the dACC and its communication with the dlPFC in cognitive control, we recorded local field potentials (LFPs) from the dlPFC before and during the reversible deactivation of the dACC, in macaque monkeys engaging in uncued switches between 2 stimulus-response rules, namely prosaccade and antisaccade. Cryogenic dACC deactivation impaired response accuracy during maintenance of—but not the initial switching to—the cognitively demanding antisaccade rule, which coincided with a reduction in task-related theta activity and the correct-error (C-E) difference in dlPFC beta-band power. During both rule switching and maintenance, dACC deactivation prolonged the animals' reaction time and reduced task-related alpha power in the dlPFC. Our findings support a role of the dACC in prefrontal oscillatory activities that are involved the maintenance of a new, challenging task rule.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In primates, both the dorsal anterior cingulate cortex (dACC) and the dorsolateral prefrontal cortex (dlPFC) are key regions of the frontoparietal cognitive control network. To study the role of the dACC and its communication with the dlPFC in cognitive control, we recorded local field potentials (LFPs) from the dlPFC before and during the reversible deactivation of the dACC, in macaque monkeys engaging in uncued switches between 2 stimulus-response rules, namely prosaccade and antisaccade. Cryogenic dACC deactivation impaired response accuracy during maintenance of—but not the initial switching to—the cognitively demanding antisaccade rule, which coincided with a reduction in task-related theta activity and the correct-error (C-E) difference in dlPFC beta-band power. During both rule switching and maintenance, dACC deactivation prolonged the animals' reaction time and reduced task-related alpha power in the dlPFC. Our findings support a role of the dACC in prefrontal oscillatory activities that are involved the maintenance of a new, challenging task rule. |
Corentin Massot; Uday K Jagadisan; Neeraj J Gandhi Communications Biology, 2 , pp. 1–14, 2019. @article{Massot2019, title = {Sensorimotor transformation elicits systematic patterns of activity along the dorsoventral extent of the superior colliculus in the macaque monkey}, author = {Corentin Massot and Uday K Jagadisan and Neeraj J Gandhi}, doi = {10.1038/s42003-019-0527-y}, year = {2019}, date = {2019-01-01}, journal = {Communications Biology}, volume = {2}, pages = {1--14}, abstract = {The superior colliculus (SC) is an excellent substrate to study sensorimotor transformations. To date, the spatial and temporal properties of population activity along its dorsoventral axis have been inferred from single electrode studies. Here, we recorded SC population activity in non-human primates using a linear multi-contact array during delayed saccade tasks. We show that during the visual epoch, information appeared first in dorsal layers and systematically later in ventral layers. During the delay period, the laminar organization of low-spiking rate activity matched that of the visual epoch. During the pre-saccadic epoch, spiking activity emerged first in a more ventral layer, ~ 100 ms before saccade onset. This buildup of activity appeared later on nearby neurons situated both dorsally and ventrally, culminating in a synchronous burst across the dorsoventral axis, ~ 28 ms before saccade onset. Collectively, these results reveal a principled spatiotemporal organization of SC population activity underlying sensorimotor transformation for the control of gaze.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The superior colliculus (SC) is an excellent substrate to study sensorimotor transformations. To date, the spatial and temporal properties of population activity along its dorsoventral axis have been inferred from single electrode studies. Here, we recorded SC population activity in non-human primates using a linear multi-contact array during delayed saccade tasks. We show that during the visual epoch, information appeared first in dorsal layers and systematically later in ventral layers. During the delay period, the laminar organization of low-spiking rate activity matched that of the visual epoch. During the pre-saccadic epoch, spiking activity emerged first in a more ventral layer, ~ 100 ms before saccade onset. This buildup of activity appeared later on nearby neurons situated both dorsally and ventrally, culminating in a synchronous burst across the dorsoventral axis, ~ 28 ms before saccade onset. Collectively, these results reveal a principled spatiotemporal organization of SC population activity underlying sensorimotor transformation for the control of gaze. |
Vincent B McGinty Overt attention toward appetitive cues enhances their subjective value, independent of orbitofrontal cortex activity Journal Article eNeuro, 6 (6), pp. 1–19, 2019. @article{McGinty2019, title = {Overt attention toward appetitive cues enhances their subjective value, independent of orbitofrontal cortex activity}, author = {Vincent B McGinty}, doi = {10.1523/ENEURO.0230-19.2019}, year = {2019}, date = {2019-01-01}, journal = {eNeuro}, volume = {6}, number = {6}, pages = {1--19}, abstract = {Neural representations of value underlie many behaviors that are crucial for survival. Previously, we found that value representations in primate orbitofrontal cortex (OFC) are modulated by attention, specifically, by overt shifts of gaze toward or away from reward-associated visual cues (McGinty et al., 2016). Here, we investigate the influence of overt attention on behavior by asking how gaze shifts correlate with reward anticipatory responses and whether activity in OFC mediates this correlation. Macaque monkeys viewed pavlovian conditioned appetitive cues on a visual display, while the fraction of time they spent looking toward or away from the cues was measured using an eye tracker. Also measured during cue presentation were the reward anticipation, indicated by conditioned licking responses (CRs), and single-neuron activity in OFC. In general, gaze allocation predicted subsequent licking responses: the longer the monkeys spent looking at a cue at a given time point in a trial, the more likely they were to produce an anticipatory CR later in that trial, as if the subjective value of the cue were increased. To address neural mechanisms, mediation analysis measured the extent to which the gaze–CR correlation could be statistically explained by the concurrently recorded firing of OFC neurons. The resulting mediation effects were indistinguishable from chance. Therefore, while overt attention may increase the subjective value of reward-associated cues (as revealed by anticipatory behaviors), the underlying mechanism remains unknown, as does the functional significance of gaze-driven modulation of OFC value signals.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neural representations of value underlie many behaviors that are crucial for survival. Previously, we found that value representations in primate orbitofrontal cortex (OFC) are modulated by attention, specifically, by overt shifts of gaze toward or away from reward-associated visual cues (McGinty et al., 2016). Here, we investigate the influence of overt attention on behavior by asking how gaze shifts correlate with reward anticipatory responses and whether activity in OFC mediates this correlation. Macaque monkeys viewed pavlovian conditioned appetitive cues on a visual display, while the fraction of time they spent looking toward or away from the cues was measured using an eye tracker. Also measured during cue presentation were the reward anticipation, indicated by conditioned licking responses (CRs), and single-neuron activity in OFC. In general, gaze allocation predicted subsequent licking responses: the longer the monkeys spent looking at a cue at a given time point in a trial, the more likely they were to produce an anticipatory CR later in that trial, as if the subjective value of the cue were increased. To address neural mechanisms, mediation analysis measured the extent to which the gaze–CR correlation could be statistically explained by the concurrently recorded firing of OFC neurons. The resulting mediation effects were indistinguishable from chance. Therefore, while overt attention may increase the subjective value of reward-associated cues (as revealed by anticipatory behaviors), the underlying mechanism remains unknown, as does the functional significance of gaze-driven modulation of OFC value signals. |
Priyanka S Mehta; Jiaxin Cindy Tu; Giuliana A LoConte; Meghan C Pesce; Benjamin Y Hayden Ventromedial prefrontal cortex tracks multiple environmental variables during search Journal Article The Journal of Neuroscience, 39 (27), pp. 5336–5350, 2019. @article{Mehta2019, title = {Ventromedial prefrontal cortex tracks multiple environmental variables during search}, author = {Priyanka S Mehta and Jiaxin Cindy Tu and Giuliana A LoConte and Meghan C Pesce and Benjamin Y Hayden}, doi = {10.1523/JNEUROSCI.2365-18.2019}, year = {2019}, date = {2019-01-01}, journal = {The Journal of Neuroscience}, volume = {39}, number = {27}, pages = {5336--5350}, abstract = {To make efficient foraging decisions, we must combine information about the values of available options with nonvalue information. Some accounts of ventromedial PFC (vmPFC) suggest that it has a narrow role limited to evaluating immediately available options. We examined responses of neurons in area 14 (a putative macaque homolog of human vmPFC) as 2 male macaques performed a novel foraging search task. Although many neurons encoded the values of immediately available offers, they also independently encoded several other variables that influence choice, but that are conceptually distinct from offer value. These variables include average reward rate, number of offers viewed per trial, previous offer values, previous outcome sizes, and the locations of the currently attended offer.We conclude that, rather than serving as specialized economic value center, vmPFC plays a broad role in integrating relevant environmental information to drive foraging decisions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } To make efficient foraging decisions, we must combine information about the values of available options with nonvalue information. Some accounts of ventromedial PFC (vmPFC) suggest that it has a narrow role limited to evaluating immediately available options. We examined responses of neurons in area 14 (a putative macaque homolog of human vmPFC) as 2 male macaques performed a novel foraging search task. Although many neurons encoded the values of immediately available offers, they also independently encoded several other variables that influence choice, but that are conceptually distinct from offer value. These variables include average reward rate, number of offers viewed per trial, previous offer values, previous outcome sizes, and the locations of the currently attended offer.We conclude that, rather than serving as specialized economic value center, vmPFC plays a broad role in integrating relevant environmental information to drive foraging decisions. |
Aidan P Murphy; David A Leopold A parameterized digital 3D model of the Rhesus macaque face for investigating the visual processing of social cues Journal Article Journal of Neuroscience Methods, 324 , pp. 1–14, 2019. @article{Murphy2019b, title = {A parameterized digital 3D model of the Rhesus macaque face for investigating the visual processing of social cues}, author = {Aidan P Murphy and David A Leopold}, doi = {10.1016/j.jneumeth.2019.06.001}, year = {2019}, date = {2019-01-01}, journal = {Journal of Neuroscience Methods}, volume = {324}, pages = {1--14}, publisher = {Elsevier}, abstract = {Background: Rhesus macaques are the most popular model species for studying the neural basis of visual face processing and social interaction using intracranial methods. However, the challenge of creating realistic, dynamic, and parametric macaque face stimuli has limited the experimental control and ethological validity of existing approaches. New method: We performed statistical analyses of in vivo computed tomography data to generate an anatomically accurate, three-dimensional representation of Rhesus macaque cranio-facial morphology. The surface structures were further edited, rigged and textured by a professional digital artist with careful reference to photographs of macaque facial expression, colouration and pelage. Results: The model offers precise, continuous, parametric control of craniofacial shape, emotional expression, head orientation, eye gaze direction, and many other parameters that can be adjusted to render either static or dynamic high-resolution faces. Example single-unit responses to such stimuli in macaque inferotemporal cortex demonstrate the value of parametric control over facial appearance and behaviours. Comparison with existing method(s): The generation of such a high-dimensionality and systematically controlled stimulus set of conspecific faces, with accurate craniofacial modelling and professional finalization of facial details, is currently not achievable using existing methods. Conclusions: The results herald a new set of possibilities in adaptive sampling of a high-dimensional and socially meaningful feature space, thus opening the door to systematic testing of hypotheses about the abundant neural specialization for faces found in the primate.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Background: Rhesus macaques are the most popular model species for studying the neural basis of visual face processing and social interaction using intracranial methods. However, the challenge of creating realistic, dynamic, and parametric macaque face stimuli has limited the experimental control and ethological validity of existing approaches. New method: We performed statistical analyses of in vivo computed tomography data to generate an anatomically accurate, three-dimensional representation of Rhesus macaque cranio-facial morphology. The surface structures were further edited, rigged and textured by a professional digital artist with careful reference to photographs of macaque facial expression, colouration and pelage. Results: The model offers precise, continuous, parametric control of craniofacial shape, emotional expression, head orientation, eye gaze direction, and many other parameters that can be adjusted to render either static or dynamic high-resolution faces. Example single-unit responses to such stimuli in macaque inferotemporal cortex demonstrate the value of parametric control over facial appearance and behaviours. Comparison with existing method(s): The generation of such a high-dimensionality and systematically controlled stimulus set of conspecific faces, with accurate craniofacial modelling and professional finalization of facial details, is currently not achievable using existing methods. Conclusions: The results herald a new set of possibilities in adaptive sampling of a high-dimensional and socially meaningful feature space, thus opening the door to systematic testing of hypotheses about the abundant neural specialization for faces found in the primate. |
Sunny Nigam; Sorin Pojoga; Valentin Dragoi Synergistic coding of visual information in columnar networks Journal Article Neuron, 104 , pp. 402–411, 2019. @article{Nigam2019, title = {Synergistic coding of visual information in columnar networks}, author = {Sunny Nigam and Sorin Pojoga and Valentin Dragoi}, doi = {10.1016/j.neuron.2019.07.006}, year = {2019}, date = {2019-01-01}, journal = {Neuron}, volume = {104}, pages = {402--411}, publisher = {Elsevier Inc.}, abstract = {Incoming stimuli are encoded collectively by populations of cortical neurons, which transmit information by using a neural code thought to be predominantly redundant. Redundant coding is widely believed to reflect a design choice whereby neurons with overlapping receptive fields sample environmental stimuli to convey similar information. Here, we performed multi-electrode laminar recordings in awake monkey V1 to report significant synergistic interactions between nearby neurons within a cortical column. These interactions are clustered non-randomly across cortical layers to form synergy and redundancy hubs. Homogeneous sub-populations comprising synergy hubs decode stimulus information significantly better compared to redundancy hubs or heterogeneous sub-populations. Mechanistically, synergistic interactions emerge from the stimulus dependence of correlated activity between neurons. Our findings suggest a refinement of the prevailing ideas regarding coding schemes in sensory cortex: columnar populations can efficiently encode information due to synergistic interactions even when receptive fields overlap and shared noise between cells is high.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Incoming stimuli are encoded collectively by populations of cortical neurons, which transmit information by using a neural code thought to be predominantly redundant. Redundant coding is widely believed to reflect a design choice whereby neurons with overlapping receptive fields sample environmental stimuli to convey similar information. Here, we performed multi-electrode laminar recordings in awake monkey V1 to report significant synergistic interactions between nearby neurons within a cortical column. These interactions are clustered non-randomly across cortical layers to form synergy and redundancy hubs. Homogeneous sub-populations comprising synergy hubs decode stimulus information significantly better compared to redundancy hubs or heterogeneous sub-populations. Mechanistically, synergistic interactions emerge from the stimulus dependence of correlated activity between neurons. Our findings suggest a refinement of the prevailing ideas regarding coding schemes in sensory cortex: columnar populations can efficiently encode information due to synergistic interactions even when receptive fields overlap and shared noise between cells is high. |
Kaiser Niknam; Amir Akbarian; Kelsey Clark; Yasin Zamani; Behrad Noudoost; Neda Nategh Characterizing and dissociating multiple time-varying modulatory computations influencing neuronal activity Journal Article 15 (9), pp. 1–38, 2019. @article{Niknam2019, title = {Characterizing and dissociating multiple time-varying modulatory computations influencing neuronal activity}, author = {Kaiser Niknam and Amir Akbarian and Kelsey Clark and Yasin Zamani and Behrad Noudoost and Neda Nategh}, doi = {10.1371/journal.pcbi.1007275}, year = {2019}, date = {2019-01-01}, booktitle = {PLoS Computational Biology}, volume = {15}, number = {9}, pages = {1--38}, abstract = {In many brain areas, sensory responses are heavily modulated by factors including attentional state, context, reward history, motor preparation, learned associations, and other cognitive variables. Modelling the effect of these modulatory factors on sensory responses has proven challenging, mostly due to the time-varying and nonlinear nature of the underlying computations. Here we present a computational model capable of capturing and dissociating multiple time-varying modulatory effects on neuronal responses on the order of milliseconds. The model's performance is tested on extrastriate perisaccadic visual responses in nonhuman primates. Visual neurons respond to stimuli presented around the time of saccades differently than during fixation. These perisaccadic changes include sensitivity to the stimuli presented at locations outside the neuron's receptive field, which suggests a contribution of multiple sources to perisaccadic response generation. Current computational approaches cannot quantitatively characterize the contribution of each modulatory source in response generation, mainly due to the very short timescale on which the saccade takes place. In this study, we use a high spatiotemporal resolution experimental paradigm along with a novel extension of the generalized linear model framework (GLM), termed the sparse-variable GLM, to allow for time-varying model parameters representing the temporal evolution of the system with a resolution on the order of milliseconds. We used this model framework to precisely map the temporal evolution of the spatiotemporal receptive field of visual neurons in the middle temporal area during the execution of a saccade. Moreover, an extended model based on a factorization of the sparse-variable GLM allowed us to disassociate and quantify the contribution of individual sources to the perisaccadic response. Our results show that our novel framework can precisely capture the changes in sensitivity of neurons around the time of saccades, and provide a general framework to quantitatively track the role of multiple modulatory sources over time.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In many brain areas, sensory responses are heavily modulated by factors including attentional state, context, reward history, motor preparation, learned associations, and other cognitive variables. Modelling the effect of these modulatory factors on sensory responses has proven challenging, mostly due to the time-varying and nonlinear nature of the underlying computations. Here we present a computational model capable of capturing and dissociating multiple time-varying modulatory effects on neuronal responses on the order of milliseconds. The model's performance is tested on extrastriate perisaccadic visual responses in nonhuman primates. Visual neurons respond to stimuli presented around the time of saccades differently than during fixation. These perisaccadic changes include sensitivity to the stimuli presented at locations outside the neuron's receptive field, which suggests a contribution of multiple sources to perisaccadic response generation. Current computational approaches cannot quantitatively characterize the contribution of each modulatory source in response generation, mainly due to the very short timescale on which the saccade takes place. In this study, we use a high spatiotemporal resolution experimental paradigm along with a novel extension of the generalized linear model framework (GLM), termed the sparse-variable GLM, to allow for time-varying model parameters representing the temporal evolution of the system with a resolution on the order of milliseconds. We used this model framework to precisely map the temporal evolution of the spatiotemporal receptive field of visual neurons in the middle temporal area during the execution of a saccade. Moreover, an extended model based on a factorization of the sparse-variable GLM allowed us to disassociate and quantify the contribution of individual sources to the perisaccadic response. Our results show that our novel framework can precisely capture the changes in sensitivity of neurons around the time of saccades, and provide a general framework to quantitatively track the role of multiple modulatory sources over time. |
Mariann Oemisch; Stephanie Westendorff; Marzyeh Azimi; Seyed Alireza Hassani; Salva Ardid; Paul Tiesinga; Thilo Womelsdorf Feature-specific prediction errors and surprise across macaque fronto-striatal circuits Journal Article Nature Communications, 10 (1), pp. 1–15, 2019. @article{Oemisch2019, title = {Feature-specific prediction errors and surprise across macaque fronto-striatal circuits}, author = {Mariann Oemisch and Stephanie Westendorff and Marzyeh Azimi and Seyed Alireza Hassani and Salva Ardid and Paul Tiesinga and Thilo Womelsdorf}, doi = {10.1038/s41467-018-08184-9}, year = {2019}, date = {2019-01-01}, journal = {Nature Communications}, volume = {10}, number = {1}, pages = {1--15}, publisher = {Springer US}, abstract = {To adjust expectations efficiently, prediction errors need to be associated with the precise features that gave rise to the unexpected outcome, but this credit assignment may be problematic if stimuli differ on multiple dimensions and it is ambiguous which feature dimension caused the outcome. Here, we report a potential solution: neurons in four recorded areas of the anterior fronto-striatal networks encode prediction errors that are specific to feature values of different dimensions of attended multidimensional stimuli. The most ubiquitous prediction error occurred for the reward-relevant dimension. Feature-specific prediction error signals a) emerge on average shortly after non-specific prediction error signals, b) arise earliest in the anterior cingulate cortex and later in dorsolateral prefrontal cortex, caudate and ventral striatum, and c) contribute to feature-based stimulus selection after learning. Thus, a widely-distributed feature-specific eligibility trace may be used to update synaptic weights for improved feature-based attention.}, keywords = {}, pubstate = {published}, tppubtype = {article} } To adjust expectations efficiently, prediction errors need to be associated with the precise features that gave rise to the unexpected outcome, but this credit assignment may be problematic if stimuli differ on multiple dimensions and it is ambiguous which feature dimension caused the outcome. Here, we report a potential solution: neurons in four recorded areas of the anterior fronto-striatal networks encode prediction errors that are specific to feature values of different dimensions of attended multidimensional stimuli. The most ubiquitous prediction error occurred for the reward-relevant dimension. Feature-specific prediction error signals a) emerge on average shortly after non-specific prediction error signals, b) arise earliest in the anterior cingulate cortex and later in dorsolateral prefrontal cortex, caudate and ventral striatum, and c) contribute to feature-based stimulus selection after learning. Thus, a widely-distributed feature-specific eligibility trace may be used to update synaptic weights for improved feature-based attention. |
Davide Paoletti; Christoph Braun; Elisabeth Julie Vargo; Wieske van Zoest Spontaneous pre-stimulus oscillatory activity shapes the way we look: A concurrent imaging and eye-movement study Journal Article European Journal of Neuroscience, 49 , pp. 137–149, 2019. @article{Paoletti2019, title = {Spontaneous pre-stimulus oscillatory activity shapes the way we look: A concurrent imaging and eye-movement study}, author = {Davide Paoletti and Christoph Braun and Elisabeth Julie Vargo and Wieske van Zoest}, doi = {10.1111/ejn.14285}, year = {2019}, date = {2019-01-01}, journal = {European Journal of Neuroscience}, volume = {49}, pages = {137--149}, abstract = {Previous behavioural studies have accrued evidence that response time plays a critical role in determining whether selection is influenced by stimulus saliency or target template. In the present work, we investigated to what extent the variations in timing and consequent oculomotor controls are influenced by spontaneous variations in pre-stimulus alpha oscillations. We recorded simultaneously brain activity using magnetoencephalography (MEG) and eye movements while participants performed a visual search task. Our results show that slower saccadic reaction times were predicted by an overall stronger alpha power in the 500 ms time window preceding the stimulus onset, while weaker alpha power was a signature of faster responses. When looking separately at performance for fast and slow responses, we found evidence for two specific sources of alpha activity predicting correct versus incorrect responses. When saccades were quickly elicited, errors were predicted by stronger alpha activity in posterior areas, comprising the angular gyrus in the temporal-parietal junction (TPJ) and possibly the lateral intraparietal area (LIP). Instead, when participants were slower in responding, an increase of alpha power in frontal eye fields (FEF), supplementary eye fields (SEF) and dorsolateral pre-frontal cortex (DLPFC) predicted erroneous saccades. In other words, oculomotor accuracy in fast responses was predicted by alpha power differences in more posterior areas, while the accuracy in slow responses was predicted by alpha power differences in frontal areas, in line with the idea that these areas may be differentially related to stimulus-driven and goal-driven control of selection.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Previous behavioural studies have accrued evidence that response time plays a critical role in determining whether selection is influenced by stimulus saliency or target template. In the present work, we investigated to what extent the variations in timing and consequent oculomotor controls are influenced by spontaneous variations in pre-stimulus alpha oscillations. We recorded simultaneously brain activity using magnetoencephalography (MEG) and eye movements while participants performed a visual search task. Our results show that slower saccadic reaction times were predicted by an overall stronger alpha power in the 500 ms time window preceding the stimulus onset, while weaker alpha power was a signature of faster responses. When looking separately at performance for fast and slow responses, we found evidence for two specific sources of alpha activity predicting correct versus incorrect responses. When saccades were quickly elicited, errors were predicted by stronger alpha activity in posterior areas, comprising the angular gyrus in the temporal-parietal junction (TPJ) and possibly the lateral intraparietal area (LIP). Instead, when participants were slower in responding, an increase of alpha power in frontal eye fields (FEF), supplementary eye fields (SEF) and dorsolateral pre-frontal cortex (DLPFC) predicted erroneous saccades. In other words, oculomotor accuracy in fast responses was predicted by alpha power differences in more posterior areas, while the accuracy in slow responses was predicted by alpha power differences in frontal areas, in line with the idea that these areas may be differentially related to stimulus-driven and goal-driven control of selection. |
Michael A Paradiso; Seth Akers-Campbell; Octavio Ruiz; James E Niemeyer; Stuart Geman; Jackson Loper Transsacadic information and corollary discharge in local field potentials of macaque V1 Journal Article Frontiers in Integrative Neuroscience, 12 , pp. 1–18, 2019. @article{Paradiso2019, title = {Transsacadic information and corollary discharge in local field potentials of macaque V1}, author = {Michael A Paradiso and Seth Akers-Campbell and Octavio Ruiz and James E Niemeyer and Stuart Geman and Jackson Loper}, doi = {10.3389/fnint.2018.00063}, year = {2019}, date = {2019-01-01}, journal = {Frontiers in Integrative Neuroscience}, volume = {12}, pages = {1--18}, abstract = {Approximately three times per second, human visual perception is interrupted by a saccadic eye movement. In addition to taking the eyes to a new location, several lines of evidence suggest that the saccades play multiple roles in visual perception. Indeed, it may be crucial that visual processing is informed about movements of the eyes in order to analyze visual input distinctly and efficiently on each fixation and preserve stable visual perception of the world across saccades. A variety of studies has demonstrated that activity in multiple brain areas is modulated by saccades. The hypothesis tested here is that these signals carry significant information that could be used in visual processing. To test this hypothesis, local field potentials (LFPs) were simultaneously recorded from multiple electrodes in macaque primary visual cortex (V1); support vector machines (SVMs) were used to classify the peri-saccadic LFPs. We find that LFPs in area V1 carry information that can be used to distinguish neural activity associated with fixations from saccades, precisely estimate the onset time of fixations, and reliably infer the directions of saccades. This information may be used by the brain in processes including visual stability, saccadic suppression, receptive field (RF) remapping, fixation amplification, and trans-saccadic visual perception.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Approximately three times per second, human visual perception is interrupted by a saccadic eye movement. In addition to taking the eyes to a new location, several lines of evidence suggest that the saccades play multiple roles in visual perception. Indeed, it may be crucial that visual processing is informed about movements of the eyes in order to analyze visual input distinctly and efficiently on each fixation and preserve stable visual perception of the world across saccades. A variety of studies has demonstrated that activity in multiple brain areas is modulated by saccades. The hypothesis tested here is that these signals carry significant information that could be used in visual processing. To test this hypothesis, local field potentials (LFPs) were simultaneously recorded from multiple electrodes in macaque primary visual cortex (V1); support vector machines (SVMs) were used to classify the peri-saccadic LFPs. We find that LFPs in area V1 carry information that can be used to distinguish neural activity associated with fixations from saccades, precisely estimate the onset time of fixations, and reliably infer the directions of saccades. This information may be used by the brain in processes including visual stability, saccadic suppression, receptive field (RF) remapping, fixation amplification, and trans-saccadic visual perception. |
Aishwarya Parthasarathy; Cheng Tang; Roger Herikstad; Loong Fah Cheong; Shih Cheng Yen; Camilo Libedinsky Time-invariant working memory representations in the presence of code-morphing in the lateral prefrontal cortex Journal Article Nature Communications, 10 , pp. 1–11, 2019. @article{Parthasarathy2019, title = {Time-invariant working memory representations in the presence of code-morphing in the lateral prefrontal cortex}, author = {Aishwarya Parthasarathy and Cheng Tang and Roger Herikstad and Loong Fah Cheong and Shih Cheng Yen and Camilo Libedinsky}, doi = {10.1038/s41467-019-12841-y}, year = {2019}, date = {2019-01-01}, journal = {Nature Communications}, volume = {10}, pages = {1--11}, publisher = {Springer US}, abstract = {Maintenance of working memory is thought to involve the activity of prefrontal neuronal populations with strong recurrent connections. However, it was recently shown that distractors evoke a morphing of the prefrontal population code, even when memories are maintained throughout the delay. How can a morphing code maintain time-invariant memory information? We hypothesized that dynamic prefrontal activity contains time-invariant memory information within a subspace of neural activity. Using an optimization algorithm, we found a low-dimensional subspace that contains time-invariant memory information. This information was reduced in trials where the animals made errors in the task, and was also found in periods of the trial not used to find the subspace. A bump attractor model replicated these properties, and provided predictions that were confirmed in the neural data. Our results suggest that the high-dimensional responses of prefrontal cortex contain subspaces where different types of information can be simultaneously encoded with minimal interference.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Maintenance of working memory is thought to involve the activity of prefrontal neuronal populations with strong recurrent connections. However, it was recently shown that distractors evoke a morphing of the prefrontal population code, even when memories are maintained throughout the delay. How can a morphing code maintain time-invariant memory information? We hypothesized that dynamic prefrontal activity contains time-invariant memory information within a subspace of neural activity. Using an optimization algorithm, we found a low-dimensional subspace that contains time-invariant memory information. This information was reduced in trials where the animals made errors in the task, and was also found in periods of the trial not used to find the subspace. A bump attractor model replicated these properties, and provided predictions that were confirmed in the neural data. Our results suggest that the high-dimensional responses of prefrontal cortex contain subspaces where different types of information can be simultaneously encoded with minimal interference. |
Alina Peter; Cem Uran; Johanna Klon-Lipok; Rasmus Roese; Sylvia Van Stijn; William Barnes; Jarrod R Dowdall; Wolf Singer; Pascal Fries; Martin Vinck Surface color and predictability determine contextual modulation of V1 firing and gamma oscillations Journal Article eLife, 8 , pp. 1–38, 2019. @article{Peter2019, title = {Surface color and predictability determine contextual modulation of V1 firing and gamma oscillations}, author = {Alina Peter and Cem Uran and Johanna Klon-Lipok and Rasmus Roese and Sylvia {Van Stijn} and William Barnes and Jarrod R Dowdall and Wolf Singer and Pascal Fries and Martin Vinck}, doi = {10.7554/eLife.42101}, year = {2019}, date = {2019-01-01}, journal = {eLife}, volume = {8}, pages = {1--38}, abstract = {The integration of direct bottom-up inputs with contextual information is a core feature of neocortical circuits. In area V1, neurons may reduce their firing rates when their receptive field input can be predicted by spatial context. Gamma-synchronized (30–80 Hz) firing may provide a complementary signal to rates, reflecting stronger synchronization between neuronal populations receiving mutually predictable inputs. We show that large uniform surfaces, which have high spatial predictability, strongly suppressed firing yet induced prominent gamma synchronization in macaque V1, particularly when they were colored. Yet, chromatic mismatches between center and surround, breaking predictability, strongly reduced gamma synchronization while increasing firing rates. Differences between responses to different colors, including strong gamma-responses to red, arose from stimulus adaptation to a full-screen background, suggesting prominent differences in adaptation between M- and L-cone signaling pathways. Thus, synchrony signaled whether RF inputs were predicted from spatial context, while firing rates increased when stimuli were unpredicted from context.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The integration of direct bottom-up inputs with contextual information is a core feature of neocortical circuits. In area V1, neurons may reduce their firing rates when their receptive field input can be predicted by spatial context. Gamma-synchronized (30–80 Hz) firing may provide a complementary signal to rates, reflecting stronger synchronization between neuronal populations receiving mutually predictable inputs. We show that large uniform surfaces, which have high spatial predictability, strongly suppressed firing yet induced prominent gamma synchronization in macaque V1, particularly when they were colored. Yet, chromatic mismatches between center and surround, breaking predictability, strongly reduced gamma synchronization while increasing firing rates. Differences between responses to different colors, including strong gamma-responses to red, arose from stimulus adaptation to a full-screen background, suggesting prominent differences in adaptation between M- and L-cone signaling pathways. Thus, synchrony signaled whether RF inputs were predicted from spatial context, while firing rates increased when stimuli were unpredicted from context. |
Dina V Popovkina; Wyeth Bair; Anitha Pasupathy Modeling diverse responses to filled and outline shapes in macaque V4 Journal Article Journal of Neurophysiology, 121 (3), pp. 1059–1077, 2019. @article{Popovkina2019, title = {Modeling diverse responses to filled and outline shapes in macaque V4}, author = {Dina V Popovkina and Wyeth Bair and Anitha Pasupathy}, doi = {10.1152/jn.00456.2018}, year = {2019}, date = {2019-01-01}, journal = {Journal of Neurophysiology}, volume = {121}, number = {3}, pages = {1059--1077}, abstract = {Visual area V4 is an important midlevel cortical processing stage that subserves object recognition in primates. Studies investigating shape coding in V4 have largely probed neuronal responses with filled shapes, i.e., shapes defined by both a boundary and an interior fill. As a result, we do not know whether form-selective V4 responses are dictated by boundary features alone or if interior fill is also important. We studied 43 V4 neurons in two male macaque monkeys ( Macaca mulatta) with a set of 362 filled shapes and their corresponding outlines to determine how interior fill modulates neuronal responses in shape-selective neurons. Only a minority of neurons exhibited similar response strength and shape preferences for filled and outline stimuli. A majority responded preferentially to one stimulus category (either filled or outline shapes) and poorly to the other. Our findings are inconsistent with predictions of the hierarchical-max (HMax) V4 model that builds form selectivity from oriented boundary features and takes little account of attributes related to object surface, such as the phase of the boundary edge. We modified the V4 HMax model to include sensitivity to interior fill by either removing phase-pooling or introducing unoriented units at the V1 level; both modifications better explained our data without increasing the number of free parameters. Overall, our results suggest that boundary orientation and interior surface information are both maintained until at least the midlevel visual representation, consistent with the idea that object fill is important for recognition and perception in natural vision.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual area V4 is an important midlevel cortical processing stage that subserves object recognition in primates. Studies investigating shape coding in V4 have largely probed neuronal responses with filled shapes, i.e., shapes defined by both a boundary and an interior fill. As a result, we do not know whether form-selective V4 responses are dictated by boundary features alone or if interior fill is also important. We studied 43 V4 neurons in two male macaque monkeys ( Macaca mulatta) with a set of 362 filled shapes and their corresponding outlines to determine how interior fill modulates neuronal responses in shape-selective neurons. Only a minority of neurons exhibited similar response strength and shape preferences for filled and outline stimuli. A majority responded preferentially to one stimulus category (either filled or outline shapes) and poorly to the other. Our findings are inconsistent with predictions of the hierarchical-max (HMax) V4 model that builds form selectivity from oriented boundary features and takes little account of attributes related to object surface, such as the phase of the boundary edge. We modified the V4 HMax model to include sensitivity to interior fill by either removing phase-pooling or introducing unoriented units at the V1 level; both modifications better explained our data without increasing the number of free parameters. Overall, our results suggest that boundary orientation and interior surface information are both maintained until at least the midlevel visual representation, consistent with the idea that object fill is important for recognition and perception in natural vision. |
Rishi Rajalingham; James J DiCarlo Reversible inactivation of different millimeter-scale regions of primate IT results in rifferent patterns of core object recognition deficits Journal Article Neuron, 102 , pp. 493–505, 2019. @article{Rajalingham2019, title = {Reversible inactivation of different millimeter-scale regions of primate IT results in rifferent patterns of core object recognition deficits}, author = {Rishi Rajalingham and James J DiCarlo}, doi = {10.1016/j.neuron.2019.02.001}, year = {2019}, date = {2019-01-01}, journal = {Neuron}, volume = {102}, pages = {493--505}, publisher = {Elsevier Inc.}, abstract = {Extensive research suggests that the inferior temporal (IT) population supports visual object recognition behavior. However, causal evidence for this hypothesis has been equivocal, particularly beyond the specific case of face-selective subregions of IT. Here, we directly tested this hypothesis by pharmacologically inactivating individual, millimeter-scale subregions of IT while monkeys performed several core object recognition subtasks, interleaved trial- by trial. First, we observed that IT inactivation resulted in reliable contralateral-biased subtask-selective behavioral deficits. Moreover, inactivating different IT subregions resulted in different patterns of subtask deficits, predicted by each subregion's neuronal object discriminability. Finally, the similarity between different inactivation effects was tightly related to the anatomical distance between corre- sponding inactivation sites. Taken together, these results provide direct evidence that the IT cortex causally supports general core object recognition and that the underlying IT coding dimensions are topographically organized.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Extensive research suggests that the inferior temporal (IT) population supports visual object recognition behavior. However, causal evidence for this hypothesis has been equivocal, particularly beyond the specific case of face-selective subregions of IT. Here, we directly tested this hypothesis by pharmacologically inactivating individual, millimeter-scale subregions of IT while monkeys performed several core object recognition subtasks, interleaved trial- by trial. First, we observed that IT inactivation resulted in reliable contralateral-biased subtask-selective behavioral deficits. Moreover, inactivating different IT subregions resulted in different patterns of subtask deficits, predicted by each subregion's neuronal object discriminability. Finally, the similarity between different inactivation effects was tightly related to the anatomical distance between corre- sponding inactivation sites. Taken together, these results provide direct evidence that the IT cortex causally supports general core object recognition and that the underlying IT coding dimensions are topographically organized. |
Douglas A Ruff; Marlene R Cohen Simultaneous multi-area recordings suggest that attention improves performance by reshaping stimulus representations Journal Article Nature Neuroscience, 22 , pp. 1669–1676, 2019. @article{Ruff2019, title = {Simultaneous multi-area recordings suggest that attention improves performance by reshaping stimulus representations}, author = {Douglas A Ruff and Marlene R Cohen}, doi = {10.1038/s41593-019-0477-1}, year = {2019}, date = {2019-01-01}, journal = {Nature Neuroscience}, volume = {22}, pages = {1669--1676}, publisher = {Springer US}, abstract = {Visual attention dramatically improves individuals' ability to see and modulates the responses of neurons in every known visual and oculomotor area, but whether such modulations can account for perceptual improvements is unclear. We measured the relationship between populations of visual neurons, oculomotor neurons and behavior during detection and discrimination tasks. We found that neither of the two prominent hypothesized neuronal mechanisms underlying attention (which concern changes in information coding and the way sensory information is read out) provide a satisfying account of the observed behavioral improvements. Instead, our results are more consistent with the hypothesis that attention reshapes the representation of attended stimuli to more effectively influence behavior. Our results suggest a path toward understanding the neural underpinnings of perception and cognition in health and disease by analyzing neuronal responses in ways that are constrained by behavior and interactions between brain areas.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual attention dramatically improves individuals' ability to see and modulates the responses of neurons in every known visual and oculomotor area, but whether such modulations can account for perceptual improvements is unclear. We measured the relationship between populations of visual neurons, oculomotor neurons and behavior during detection and discrimination tasks. We found that neither of the two prominent hypothesized neuronal mechanisms underlying attention (which concern changes in information coding and the way sensory information is read out) provide a satisfying account of the observed behavioral improvements. Instead, our results are more consistent with the hypothesis that attention reshapes the representation of attended stimuli to more effectively influence behavior. Our results suggest a path toward understanding the neural underpinnings of perception and cognition in health and disease by analyzing neuronal responses in ways that are constrained by behavior and interactions between brain areas. |
Amirsaman Sajad; David C Godlove; Jeffrey D Schall Cortical microcircuitry of performance monitoring Journal Article Nature Neuroscience, 22 , pp. 265–274, 2019. @article{Sajad2019, title = {Cortical microcircuitry of performance monitoring}, author = {Amirsaman Sajad and David C Godlove and Jeffrey D Schall}, doi = {10.1038/s41593-018-0309-8}, year = {2019}, date = {2019-01-01}, journal = {Nature Neuroscience}, volume = {22}, pages = {265--274}, publisher = {Springer US}, abstract = {The medial frontal cortex enables performance monitoring, indexed by the error-related negativity (ERN) and manifested by performance adaptations. We recorded electroencephalogram over and neural spiking across all layers of the supplementary eye field, an agranular cortical area, in monkeys performing a saccade-countermanding (stop signal) task. Neurons signaling error production, feedback predicting reward gain or loss, and delivery of fluid reward had different spike widths and were concentrated differently across layers. Neurons signaling error or loss of reward were more common in layers 2 and 3 (L2/3), whereas neurons signaling gain of reward were more common in layers 5 and 6 (L5/6). Variation of error– and reinforcement-related spike rates in L2/3 but not L5/6 predicted response time adaptation. Variation in error-related spike rate in L2/3 but not L5/6 predicted ERN magnitude. These findings reveal novel features of cortical microcircuitry supporting performance monitoring and confirm one cortical source of the ERN.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The medial frontal cortex enables performance monitoring, indexed by the error-related negativity (ERN) and manifested by performance adaptations. We recorded electroencephalogram over and neural spiking across all layers of the supplementary eye field, an agranular cortical area, in monkeys performing a saccade-countermanding (stop signal) task. Neurons signaling error production, feedback predicting reward gain or loss, and delivery of fluid reward had different spike widths and were concentrated differently across layers. Neurons signaling error or loss of reward were more common in layers 2 and 3 (L2/3), whereas neurons signaling gain of reward were more common in layers 5 and 6 (L5/6). Variation of error– and reinforcement-related spike rates in L2/3 but not L5/6 predicted response time adaptation. Variation in error-related spike rate in L2/3 but not L5/6 predicted ERN magnitude. These findings reveal novel features of cortical microcircuitry supporting performance monitoring and confirm one cortical source of the ERN. |
Jason M Samonds; Veronica Choi; Nicholas J Priebe Mice discriminate stereoscopic surfaces without fixating in depth Journal Article The Journal of Neuroscience, 39 (41), pp. 8024–8037, 2019. @article{Samonds2019, title = {Mice discriminate stereoscopic surfaces without fixating in depth}, author = {Jason M Samonds and Veronica Choi and Nicholas J Priebe}, doi = {10.1523/JNEUROSCI.0895-19.2019}, year = {2019}, date = {2019-01-01}, journal = {The Journal of Neuroscience}, volume = {39}, number = {41}, pages = {8024--8037}, abstract = {Stereopsis is aubiquitous feature ofprimatemammalianvision, but little is knownabout ifandhowrodentssuchasmiceuse stereoscopic vision. We used random dot stereograms to test for stereopsis in male and female mice, and they were able to discriminate near from far surfaces over a range of disparities, with diminishing performance for small and large binocular disparities. Based on two-photon measurements of disparity tuning, the range of disparities represented in the visual cortex aligns with the behavior and covers a broad range ofdisparities. Whenwe examined their binocular eye movements, we found that, unlike primates, mice did not systematically vary relative eye positions or use vergence eye movements when presented with different disparities. Nonetheless, the representation of disparity tuning was wide enough to capture stereoscopic information over a range of potential vergence angles. Although mice share fundamental characteristics of stereoscopic vision with primates and carnivores, their lack ofdisparity-dependent vergence eye move- ments and wide neuronal representation suggests that they may use a distinct strategy for stereopsis.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Stereopsis is aubiquitous feature ofprimatemammalianvision, but little is knownabout ifandhowrodentssuchasmiceuse stereoscopic vision. We used random dot stereograms to test for stereopsis in male and female mice, and they were able to discriminate near from far surfaces over a range of disparities, with diminishing performance for small and large binocular disparities. Based on two-photon measurements of disparity tuning, the range of disparities represented in the visual cortex aligns with the behavior and covers a broad range ofdisparities. Whenwe examined their binocular eye movements, we found that, unlike primates, mice did not systematically vary relative eye positions or use vergence eye movements when presented with different disparities. Nonetheless, the representation of disparity tuning was wide enough to capture stereoscopic information over a range of potential vergence angles. Although mice share fundamental characteristics of stereoscopic vision with primates and carnivores, their lack ofdisparity-dependent vergence eye move- ments and wide neuronal representation suggests that they may use a distinct strategy for stereopsis. |
Morteza Sarafyazd; Mehrdad Jazayeri Hierarchical reasoning by neural circuits in the frontal cortex Journal Article Science, 364 , pp. 1–11, 2019. @article{Sarafyazd2019, title = {Hierarchical reasoning by neural circuits in the frontal cortex}, author = {Morteza Sarafyazd and Mehrdad Jazayeri}, doi = {10.1126/science.aav8911}, year = {2019}, date = {2019-01-01}, journal = {Science}, volume = {364}, pages = {1--11}, abstract = {Humans process information hierarchically. In the presence of hierarchies, sources of failures are ambiguous. Humans resolve this ambiguity by assessing their confidence after one or more attempts. To understand the neural basis of this reasoning strategy, we recorded from dorsomedial frontal cortex (DMFC) and anterior cingulate cortex (ACC) of monkeys in a task in which negative outcomes were caused either by misjudging the stimulus or by a covert switch between two stimulus-response contingency rules. We found that both areas harbored a representation of evidence supporting a rule switch. Additional perturbation experiments revealed that ACC functioned downstream of DMFC and was directly and specifically involved in inferring covert rule switches. These results reveal the computational principles of hierarchical reasoning, as implemented by cortical circuits.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Humans process information hierarchically. In the presence of hierarchies, sources of failures are ambiguous. Humans resolve this ambiguity by assessing their confidence after one or more attempts. To understand the neural basis of this reasoning strategy, we recorded from dorsomedial frontal cortex (DMFC) and anterior cingulate cortex (ACC) of monkeys in a task in which negative outcomes were caused either by misjudging the stimulus or by a covert switch between two stimulus-response contingency rules. We found that both areas harbored a representation of evidence supporting a rule switch. Additional perturbation experiments revealed that ACC functioned downstream of DMFC and was directly and specifically involved in inferring covert rule switches. These results reveal the computational principles of hierarchical reasoning, as implemented by cortical circuits. |
Veronica E Scerra; M Gabriela Costello; Emilio Salinas; Terrence R Stanford All-or-none context dependence delineates limits of FEF visual target selection Journal Article Current Biology, 29 , pp. 294–305, 2019. @article{Scerra2019, title = {All-or-none context dependence delineates limits of FEF visual target selection}, author = {Veronica E Scerra and M {Gabriela Costello} and Emilio Salinas and Terrence R Stanford}, doi = {10.1016/j.cub.2018.12.013}, year = {2019}, date = {2019-01-01}, journal = {Current Biology}, volume = {29}, pages = {294--305}, abstract = {Choices of where to look are informed by perceptual judgments, which locate objects of current value or interest within the visual scene. This perceptual-motor transform is partly implemented in the frontal eye field (FEF), where visually responsive neurons appear to select behaviorally relevant visual targets and, subsequently, saccade-related neurons select the movements required to look at them. Here, we use urgent decision-making tasks to show (1) that FEF motor activity can direct accurate, visually informed choices in the complete absence of prior target-distracter discrimination by FEF visual responses and (2) that such discrimination by FEF visual cells shows an all-or-none reliance on the presence of stimulus attributes strongly associated with saliency-driven attentional allocation. The present findings suggest that FEF visual target selection is specific to visual judgments made on the basis of saliency and may not play a significant role in guiding saccadic choices informed solely by feature content.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Choices of where to look are informed by perceptual judgments, which locate objects of current value or interest within the visual scene. This perceptual-motor transform is partly implemented in the frontal eye field (FEF), where visually responsive neurons appear to select behaviorally relevant visual targets and, subsequently, saccade-related neurons select the movements required to look at them. Here, we use urgent decision-making tasks to show (1) that FEF motor activity can direct accurate, visually informed choices in the complete absence of prior target-distracter discrimination by FEF visual responses and (2) that such discrimination by FEF visual cells shows an all-or-none reliance on the presence of stimulus attributes strongly associated with saliency-driven attentional allocation. The present findings suggest that FEF visual target selection is specific to visual judgments made on the basis of saliency and may not play a significant role in guiding saccadic choices informed solely by feature content. |
Ehsan Sedaghat-Nejad; David J Herzfeld; Paul Hage; Kaveh Karbasi; Tara Palin; Xiaoqin Wang; Reza Shadmehr Behavioral training of marmosets and electrophysiological recording from the cerebellum Journal Article 122 (4), pp. 1502–1517, 2019. @article{Sedaghat-Nejad2019, title = {Behavioral training of marmosets and electrophysiological recording from the cerebellum}, author = {Ehsan Sedaghat-Nejad and David J Herzfeld and Paul Hage and Kaveh Karbasi and Tara Palin and Xiaoqin Wang and Reza Shadmehr}, doi = {10.1152/jn.00389.2019}, year = {2019}, date = {2019-01-01}, booktitle = {Journal of Neurophysiology}, volume = {122}, number = {4}, pages = {1502--1517}, abstract = {The common marmoset (Callithrix jacchus) is a promising new model for study of neurophysiological basis of behavior in primates. Like other primates, it relies on saccadic eye movements to monitor and explore its environment. Previous reports have demonstrated some success in training marmosets to produce goal-directed actions in the laboratory. However, the number of trials per session has been relatively small, thus limiting the utility of marmosets as a model for behavioral and neurophysiological studies. In this article, we report the results of a series of new behavioral training and neurophysiological protocols aimed at increasing the number of trials per session while recording from the cerebellum. To improve the training efficacy, we designed a precisely calibrated food regulation regime that motivates the subjects to perform saccade tasks, resulting in ~1,000 reward-driven trials on a daily basis. We then developed a multichannel recording system that uses imaging to target a desired region of the cerebellum, allowing for simultaneous isolation of multiple Purkinje cells in the vermis. In this report, we describe 1) the design and surgical implantation of a computer tomography (CT)guided, subject-specific head post, 2) the design of a CT- and MRI-guided alignment tool for trajectory guidance of electrodes mounted on an absolute encoder microdrive, 3) development of a protocol for behavioral training of subjects, and 4) simultaneous recordings from pairs of Purkinje cells during a saccade task.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The common marmoset (Callithrix jacchus) is a promising new model for study of neurophysiological basis of behavior in primates. Like other primates, it relies on saccadic eye movements to monitor and explore its environment. Previous reports have demonstrated some success in training marmosets to produce goal-directed actions in the laboratory. However, the number of trials per session has been relatively small, thus limiting the utility of marmosets as a model for behavioral and neurophysiological studies. In this article, we report the results of a series of new behavioral training and neurophysiological protocols aimed at increasing the number of trials per session while recording from the cerebellum. To improve the training efficacy, we designed a precisely calibrated food regulation regime that motivates the subjects to perform saccade tasks, resulting in ~1,000 reward-driven trials on a daily basis. We then developed a multichannel recording system that uses imaging to target a desired region of the cerebellum, allowing for simultaneous isolation of multiple Purkinje cells in the vermis. In this report, we describe 1) the design and surgical implantation of a computer tomography (CT)guided, subject-specific head post, 2) the design of a CT- and MRI-guided alignment tool for trajectory guidance of electrodes mounted on an absolute encoder microdrive, 3) development of a protocol for behavioral training of subjects, and 4) simultaneous recordings from pairs of Purkinje cells during a saccade task. |
Janahan Selvanayagam; Kevin D Johnston; David J Schaeffer; Lauren K Hayrynen; Stefan Everling Functional localization of the frontal eye fields in the common marmoset using microstimulation Journal Article The Journal of Neuroscience, 39 (46), pp. 9197–9206, 2019. @article{Selvanayagam2019, title = {Functional localization of the frontal eye fields in the common marmoset using microstimulation}, author = {Janahan Selvanayagam and Kevin D Johnston and David J Schaeffer and Lauren K Hayrynen and Stefan Everling}, doi = {10.1523/JNEUROSCI.1786-19.2019}, year = {2019}, date = {2019-01-01}, journal = {The Journal of Neuroscience}, volume = {39}, number = {46}, pages = {9197--9206}, abstract = {The frontal eye field (FEF) is a critical region for the deployment of overt and covert spatial attention. Although investigations in the macaque continue to provide insight into the neural underpinnings of the FEF, due to its location within a sulcus, the macaque FEF is virtually inaccessible to electrophysiological techniques such as high-density and laminar recordings. With a largely lissencephalic cortex, the common marmoset (Callithrix jacchus) is a promising alternative primate model for studying FEF microcircuitry. Putative homologies have been established with the macaque FEF on the basis of cytoarchitecture and connectivity; however, physiological investigation in awake, behaving marmosets is necessary to physiologically locate this area. Here, we addressed this gap using intracortical microstimulation in a broad range of frontal cortical areas in three adult marmosets (two males, one female). We implanted marmosets with 96-channel Utah arrays and applied microstimulation trains while they freely viewed video clips. We evoked short-latency fixed vector saccades at low currents (textless50 $mu$A) in areas 45, 8aV, 8C, and 6DR. We observed a topography of saccade direction and amplitude consistent with findings in macaques and humans: small saccades in ventrolateral FEF and large saccades combined with contralateral neck and shoulder movements encoded in dorsomedial FEF. Our data provide compelling evidence supporting homology between marmoset and macaque FEF and suggest that the marmoset is a useful primate model for investigating FEF microcircuitry and its contributions to oculomotor and cognitive functions.SIGNIFICANCE STATEMENT The frontal eye field (FEF) is a critical cortical region for overt and covert spatial attention. The microcircuitry of this area remains poorly understood because in the macaque, the most commonly used model, it is embedded within a sulcus and is inaccessible to modern electrophysiological and imaging techniques. The common marmoset is a promising alternative primate model due to its lissencephalic cortex and potential for genetic manipulation. However, evidence for homologous cortical areas in this model remains limited and unclear. Here, we applied microstimulation in frontal cortical areas in marmosets to physiologically identify FEF. Our results provide compelling evidence for an FEF in the marmoset and suggest that the marmoset is a useful model for investigating FEF microcircuitry.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The frontal eye field (FEF) is a critical region for the deployment of overt and covert spatial attention. Although investigations in the macaque continue to provide insight into the neural underpinnings of the FEF, due to its location within a sulcus, the macaque FEF is virtually inaccessible to electrophysiological techniques such as high-density and laminar recordings. With a largely lissencephalic cortex, the common marmoset (Callithrix jacchus) is a promising alternative primate model for studying FEF microcircuitry. Putative homologies have been established with the macaque FEF on the basis of cytoarchitecture and connectivity; however, physiological investigation in awake, behaving marmosets is necessary to physiologically locate this area. Here, we addressed this gap using intracortical microstimulation in a broad range of frontal cortical areas in three adult marmosets (two males, one female). We implanted marmosets with 96-channel Utah arrays and applied microstimulation trains while they freely viewed video clips. We evoked short-latency fixed vector saccades at low currents (textless50 $mu$A) in areas 45, 8aV, 8C, and 6DR. We observed a topography of saccade direction and amplitude consistent with findings in macaques and humans: small saccades in ventrolateral FEF and large saccades combined with contralateral neck and shoulder movements encoded in dorsomedial FEF. Our data provide compelling evidence supporting homology between marmoset and macaque FEF and suggest that the marmoset is a useful primate model for investigating FEF microcircuitry and its contributions to oculomotor and cognitive functions.SIGNIFICANCE STATEMENT The frontal eye field (FEF) is a critical cortical region for overt and covert spatial attention. The microcircuitry of this area remains poorly understood because in the macaque, the most commonly used model, it is embedded within a sulcus and is inaccessible to modern electrophysiological and imaging techniques. The common marmoset is a promising alternative primate model due to its lissencephalic cortex and potential for genetic manipulation. However, evidence for homologous cortical areas in this model remains limited and unclear. Here, we applied microstimulation in frontal cortical areas in marmosets to physiologically identify FEF. Our results provide compelling evidence for an FEF in the marmoset and suggest that the marmoset is a useful model for investigating FEF microcircuitry. |
Neda Shahidi; Ariana R Andrei; Ming Hu; Valentin Dragoi High-order coordination of cortical spiking activity modulates perceptual accuracy Journal Article Nature Neuroscience, 22 , pp. 1148–1158, 2019. @article{Shahidi2019, title = {High-order coordination of cortical spiking activity modulates perceptual accuracy}, author = {Neda Shahidi and Ariana R Andrei and Ming Hu and Valentin Dragoi}, doi = {10.1038/s41593-019-0406-3}, year = {2019}, date = {2019-01-01}, journal = {Nature Neuroscience}, volume = {22}, pages = {1148--1158}, publisher = {Springer US}, abstract = {The accurate relay of electrical signals within cortical networks is key to perception and cognitive function. Theoretically, it has long been proposed that temporal coordination of neuronal spiking activity controls signal transmission and behavior. However, whether and how temporally precise neuronal coordination in population activity influences perception are unknown. Here, we recorded populations of neurons in early and mid-level visual cortex (areas V1 and V4) simultaneously to discover that the precise temporal coordination between the spiking activity of three or more cells carries information about visual perception in the absence of firing rate modulation. The accuracy of perceptual responses correlated with high-order spiking coordination within V4, but not V1, and with feedforward coordination between V1 and V4. These results indicate that while visual stimuli are encoded in the discharge rates of neurons, perceptual accuracy is related to temporally precise spiking coordination within and between cortical networks.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The accurate relay of electrical signals within cortical networks is key to perception and cognitive function. Theoretically, it has long been proposed that temporal coordination of neuronal spiking activity controls signal transmission and behavior. However, whether and how temporally precise neuronal coordination in population activity influences perception are unknown. Here, we recorded populations of neurons in early and mid-level visual cortex (areas V1 and V4) simultaneously to discover that the precise temporal coordination between the spiking activity of three or more cells carries information about visual perception in the absence of firing rate modulation. The accuracy of perceptual responses correlated with high-order spiking coordination within V4, but not V1, and with feedforward coordination between V1 and V4. These results indicate that while visual stimuli are encoded in the discharge rates of neurons, perceptual accuracy is related to temporally precise spiking coordination within and between cortical networks. |
Hansem Sohn; Devika Narain; Nicolas Meirhaeghe; Mehrdad Jazayeri Bayesian computation through cortical latent dynamics Journal Article Neuron, 103 , pp. 934–947, 2019. @article{Sohn2019, title = {Bayesian computation through cortical latent dynamics}, author = {Hansem Sohn and Devika Narain and Nicolas Meirhaeghe and Mehrdad Jazayeri}, doi = {10.1016/j.neuron.2019.06.012}, year = {2019}, date = {2019-01-01}, journal = {Neuron}, volume = {103}, pages = {934--947}, publisher = {Elsevier Inc.}, abstract = {Statistical regularities in the environment create prior beliefs that we rely on to optimize our behavior when sensory information is uncertain. Bayesian theory formalizes how prior beliefs can be leveraged and has had a major impact on models of perception, sensorimotor function, and cognition. However, it is not known how recurrent interactions among neurons mediate Bayesian integration. By using a time-interval reproduction task in monkeys, we found that prior statistics warp neural representations in the frontal cortex, allowing the mapping of sensory inputs to motor outputs to incorporate prior statistics in accordance with Bayesian inference. Analysis of recurrent neural network models performing the task revealed that this warping was enabled by a low-dimensional curved manifold and allowed us to further probe the potential causal underpinnings of this computational strategy. These results uncover a simple and general principle whereby prior beliefs exert their influence on behavior by sculpting cortical latent dynamics.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Statistical regularities in the environment create prior beliefs that we rely on to optimize our behavior when sensory information is uncertain. Bayesian theory formalizes how prior beliefs can be leveraged and has had a major impact on models of perception, sensorimotor function, and cognition. However, it is not known how recurrent interactions among neurons mediate Bayesian integration. By using a time-interval reproduction task in monkeys, we found that prior statistics warp neural representations in the frontal cortex, allowing the mapping of sensory inputs to motor outputs to incorporate prior statistics in accordance with Bayesian inference. Analysis of recurrent neural network models performing the task revealed that this warping was enabled by a low-dimensional curved manifold and allowed us to further probe the potential causal underpinnings of this computational strategy. These results uncover a simple and general principle whereby prior beliefs exert their influence on behavior by sculpting cortical latent dynamics. |
Sébastien Tremblay; Florian Pieper; Adam Sachs; Ridha Joober; Julio Martinez-Trujillo The effects of methylphenidate (Ritalin) on the neurophysiology of the monkey caudal prefrontal cortex Journal Article eNeuro, 6 (1), pp. 1–17, 2019. @article{Tremblay2019, title = {The effects of methylphenidate (Ritalin) on the neurophysiology of the monkey caudal prefrontal cortex}, author = {Sébastien Tremblay and Florian Pieper and Adam Sachs and Ridha Joober and Julio Martinez-Trujillo}, doi = {10.1523/ENEURO.0371-18.2018}, year = {2019}, date = {2019-01-01}, journal = {eNeuro}, volume = {6}, number = {1}, pages = {1--17}, abstract = {Methylphenidate (MPH), commonly known as Ritalin, is the most widely prescribed drug worldwide to treat patients with attention deficit disorders. Although MPH is thought to modulate catecholamine neurotransmission in the brain, it remains unclear how these neurochemical effects influence neuronal activity and lead to attentional enhancements. Studies in rodents overwhelmingly point to the lateral prefrontal cortex (LPFC) as a main site of action of MPH. To understand the mechanism of action of MPH in a primate brain, we recorded the responses of neuronal populations using chronic multielectrode arrays implanted in the caudal LPFC of two macaque monkeys while the animals performed an attention task (N 2811 neuronal recordings). Over different recording sessions (N 55), we orally administered either various doses of MPH or a placebo to the animals. Behavioral analyses revealed positive effects of MPH on task performance at specific doses. However, analyses of individual neurons activity, noise correlations, and neuronal ensemble activity using machine learning algorithms revealed no effects of MPH. Our results suggest that the positive behavioral effects of MPH observed in primates (including humans) may not be mediated by changes in the activity of caudal LPFC neurons. MPH may enhance cognitive performance by modulating neuronal activity in other regions of the attentional network in the primate brain.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Methylphenidate (MPH), commonly known as Ritalin, is the most widely prescribed drug worldwide to treat patients with attention deficit disorders. Although MPH is thought to modulate catecholamine neurotransmission in the brain, it remains unclear how these neurochemical effects influence neuronal activity and lead to attentional enhancements. Studies in rodents overwhelmingly point to the lateral prefrontal cortex (LPFC) as a main site of action of MPH. To understand the mechanism of action of MPH in a primate brain, we recorded the responses of neuronal populations using chronic multielectrode arrays implanted in the caudal LPFC of two macaque monkeys while the animals performed an attention task (N 2811 neuronal recordings). Over different recording sessions (N 55), we orally administered either various doses of MPH or a placebo to the animals. Behavioral analyses revealed positive effects of MPH on task performance at specific doses. However, analyses of individual neurons activity, noise correlations, and neuronal ensemble activity using machine learning algorithms revealed no effects of MPH. Our results suggest that the positive behavioral effects of MPH observed in primates (including humans) may not be mediated by changes in the activity of caudal LPFC neurons. MPH may enhance cognitive performance by modulating neuronal activity in other regions of the attentional network in the primate brain. |
Kasper Vinken; Rufin Vogels A behavioral face preference deficit in a monkey with an incomplete face patch system Journal Article NeuroImage, 189 , pp. 415–424, 2019. @article{Vinken2019, title = {A behavioral face preference deficit in a monkey with an incomplete face patch system}, author = {Kasper Vinken and Rufin Vogels}, doi = {10.1016/j.neuroimage.2019.01.043}, year = {2019}, date = {2019-01-01}, journal = {NeuroImage}, volume = {189}, pages = {415--424}, abstract = {Primates are experts in face perception and naturally show a preference for faces under free-viewing conditions. The primate ventral stream is characterized by a network of face patches that selectively responds to faces, but it remains uncertain how important such parcellation is for face perception. Here we investigated free-viewing behavior in a female monkey who naturally lacks fMRI-defined posterior and middle lateral face patches. We presented a series of content-rich images of scenes that included faces or other objects to that monkey during a free-viewing task and tested a group of 10 control monkeys on the same task for comparison. We found that, compared to controls, the monkey with missing face patches showed a marked reduction of face viewing preference that was most pronounced for the first few fixations. In addition, her gaze fixation patterns were substantially distinct from those of controls, especially for pictures with a face. These data demonstrate an association between the clustering of neurons in face selective patches and a behavioral bias for faces in natural images.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Primates are experts in face perception and naturally show a preference for faces under free-viewing conditions. The primate ventral stream is characterized by a network of face patches that selectively responds to faces, but it remains uncertain how important such parcellation is for face perception. Here we investigated free-viewing behavior in a female monkey who naturally lacks fMRI-defined posterior and middle lateral face patches. We presented a series of content-rich images of scenes that included faces or other objects to that monkey during a free-viewing task and tested a group of 10 control monkeys on the same task for comparison. We found that, compared to controls, the monkey with missing face patches showed a marked reduction of face viewing preference that was most pronounced for the first few fixations. In addition, her gaze fixation patterns were substantially distinct from those of controls, especially for pictures with a face. These data demonstrate an association between the clustering of neurons in face selective patches and a behavioral bias for faces in natural images. |
Pascal Wallisch; J Anthony Movshon Responses of neurons in macaque MT to unikinetic plaids Journal Article Journal of Neurophysiology, 122 (5), pp. 1937–1945, 2019. @article{Wallisch2019, title = {Responses of neurons in macaque MT to unikinetic plaids}, author = {Pascal Wallisch and J {Anthony Movshon}}, doi = {10.1152/jn.00486.2019}, year = {2019}, date = {2019-01-01}, journal = {Journal of Neurophysiology}, volume = {122}, number = {5}, pages = {1937--1945}, abstract = {Response properties of MT neurons are often studied with “bikinetic” plaid stimuli, which consist of two superimposed sine wave gratings moving in different directions. Oculomotor studies using “unikinetic plaids” in which only one of the two superimposed gratings moves suggest that the eyes first move reflexively in the direction of the moving grating and only later converge on the perceived direction of the moving pattern. MT has been implicated as the source of visual signals that drives these responses. We wanted to know whether stationary gratings, which have little effect on MT cells when presented alone, would influence MT responses when paired with a moving grating. We recorded extracellularly from neurons in area MT and measured responses to stationary and moving gratings, and to their sums: bikinetic and unikinetic plaids. As expected, stationary gratings presented alone had a very modest influence on the activity of MT neurons. Responses to moving gratings and bikinetic plaids were similar to those previously reported and revealed cells selective for the motion of plaid patterns and of their components (pattern and component cells). When these neurons were probed with unikinetic plaids, pattern cells shifted their direction preferences in a way that revealed the influence of the static grating. Component cell preferences shifted little or not at all. These results support the notion that pattern-selective neurons in area MT integrate component motions that differ widely in speed, and that they do so in a way that is consistent with an intersection-of-constraints model.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Response properties of MT neurons are often studied with “bikinetic” plaid stimuli, which consist of two superimposed sine wave gratings moving in different directions. Oculomotor studies using “unikinetic plaids” in which only one of the two superimposed gratings moves suggest that the eyes first move reflexively in the direction of the moving grating and only later converge on the perceived direction of the moving pattern. MT has been implicated as the source of visual signals that drives these responses. We wanted to know whether stationary gratings, which have little effect on MT cells when presented alone, would influence MT responses when paired with a moving grating. We recorded extracellularly from neurons in area MT and measured responses to stationary and moving gratings, and to their sums: bikinetic and unikinetic plaids. As expected, stationary gratings presented alone had a very modest influence on the activity of MT neurons. Responses to moving gratings and bikinetic plaids were similar to those previously reported and revealed cells selective for the motion of plaid patterns and of their components (pattern and component cells). When these neurons were probed with unikinetic plaids, pattern cells shifted their direction preferences in a way that revealed the influence of the static grating. Component cell preferences shifted little or not at all. These results support the notion that pattern-selective neurons in area MT integrate component motions that differ widely in speed, and that they do so in a way that is consistent with an intersection-of-constraints model. |
Maya Zhe Wang; Benjamin Y Hayden Monkeys are curious about counterfactual outcomes Journal Article Cognition, 189 , pp. 1–10, 2019. @article{Wang2019g, title = {Monkeys are curious about counterfactual outcomes}, author = {Maya Zhe Wang and Benjamin Y Hayden}, doi = {10.1016/j.cognition.2019.03.009}, year = {2019}, date = {2019-01-01}, journal = {Cognition}, volume = {189}, pages = {1--10}, publisher = {Elsevier}, abstract = {Many non-human animals show exploratory behaviors. It remains unclear whether any possess human-like curiosity. We previously proposed three criteria for applying the term curiosity to animal behavior: (1) the subject is willing to sacrifice reward to obtain information, (2) the information provides no immediate instrumental or strategic benefit, and (3) the amount the subject is willing to pay depends systematically on the amount of information available. In previous work on information-seeking in animals, information generally predicts upcoming rewards, and animals' decisions may therefore be a byproduct of reinforcement processes. Here we get around this potential confound by taking advantage of macaques' ability to reason counterfactually (that is, about outcomes that could have occurred had the subject chosen differently). Specifically, macaques sacrificed fluid reward to obtain information about counterfactual outcomes. Moreover, their willingness to pay scaled with the information (Shannon entropy) offered by the counterfactual option. These results demonstrate the existence of human-like curiosity in non-human primates according to our criteria, which circumvent several confounds associated with less stringent criteria.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Many non-human animals show exploratory behaviors. It remains unclear whether any possess human-like curiosity. We previously proposed three criteria for applying the term curiosity to animal behavior: (1) the subject is willing to sacrifice reward to obtain information, (2) the information provides no immediate instrumental or strategic benefit, and (3) the amount the subject is willing to pay depends systematically on the amount of information available. In previous work on information-seeking in animals, information generally predicts upcoming rewards, and animals' decisions may therefore be a byproduct of reinforcement processes. Here we get around this potential confound by taking advantage of macaques' ability to reason counterfactually (that is, about outcomes that could have occurred had the subject chosen differently). Specifically, macaques sacrificed fluid reward to obtain information about counterfactual outcomes. Moreover, their willingness to pay scaled with the information (Shannon entropy) offered by the counterfactual option. These results demonstrate the existence of human-like curiosity in non-human primates according to our criteria, which circumvent several confounds associated with less stringent criteria. |
Jacob A Westerberg; Michele A Cox; Kacie Dougherty; Alexander Maier V1 microcircuit dynamics: Altered signal propagation suggests intracortical origins for adaptation in response to visual repetition Journal Article Journal of Neurophysiology, 121 (5), pp. 1938–1952, 2019. @article{Westerberg2019, title = {V1 microcircuit dynamics: Altered signal propagation suggests intracortical origins for adaptation in response to visual repetition}, author = {Jacob A Westerberg and Michele A Cox and Kacie Dougherty and Alexander Maier}, doi = {10.1152/jn.00113.2019}, year = {2019}, date = {2019-01-01}, journal = {Journal of Neurophysiology}, volume = {121}, number = {5}, pages = {1938--1952}, abstract = {Repetitive visual stimulation profoundly changes sensory processing in the primary visual cortex (V1). We show how the associated adaptive changes are linked to an altered flow of synaptic activation across the V1 laminar microcircuit. Using repeated visual stimulation, we recorded layer-specific responses in V1 of two fixating monkeys. We found that repetition-related spiking suppression was most pronounced outside granular V1 layers that receive the main retinogeniculate input. This repetition-related response suppression was robust to alternating stimuli between the eyes, in line with the notion that repetition-related adaptation is predominantly of cortical origin. Most importantly, current source density (CSD) analysis, which provides an estimate of local net depolarization, revealed that synaptic processing during repeated stimulation was most profoundly affected within supragranular layers, which harbor the bulk of corticocortical connections. Direct comparison of the temporal evolution of laminar CSD and spiking activity showed that stimulus repetition first affected supragranular synaptic currents, which translated into a reduction of stimulus-evoked spiking across layers. Together, these results suggest that repetition induces an altered state of intracortical processing that underpins visual adaptation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Repetitive visual stimulation profoundly changes sensory processing in the primary visual cortex (V1). We show how the associated adaptive changes are linked to an altered flow of synaptic activation across the V1 laminar microcircuit. Using repeated visual stimulation, we recorded layer-specific responses in V1 of two fixating monkeys. We found that repetition-related spiking suppression was most pronounced outside granular V1 layers that receive the main retinogeniculate input. This repetition-related response suppression was robust to alternating stimuli between the eyes, in line with the notion that repetition-related adaptation is predominantly of cortical origin. Most importantly, current source density (CSD) analysis, which provides an estimate of local net depolarization, revealed that synaptic processing during repeated stimulation was most profoundly affected within supragranular layers, which harbor the bulk of corticocortical connections. Direct comparison of the temporal evolution of laminar CSD and spiking activity showed that stimulus repetition first affected supragranular synaptic currents, which translated into a reduction of stimulus-evoked spiking across layers. Together, these results suggest that repetition induces an altered state of intracortical processing that underpins visual adaptation. |
Brian J White; Laurent Itti; Douglas P Munoz Superior colliculus encodes visual saliency during smooth pursuit eye movements Journal Article European Journal of Neuroscience, pp. 1–11, 2019. @article{White2019a, title = {Superior colliculus encodes visual saliency during smooth pursuit eye movements}, author = {Brian J White and Laurent Itti and Douglas P Munoz}, doi = {10.1111/ejn.14432}, year = {2019}, date = {2019-01-01}, journal = {European Journal of Neuroscience}, pages = {1--11}, abstract = {The saliency map has played a long-standing role in models and theories of visual attention, and it is now supported by neurobiological evidence from several cortical and subcortical brain areas. While visual saliency is computed during moments of active fixation, it is not known whether the same is true while engaged in smooth pursuit of a moving stimulus, which is very common in real-world vision. Here, we examined extrafoveal saliency coding in the superior colliculus, a midbrain area associated with attention and gaze, during smooth pursuit eye movements. We found that SC neurons from the superficial visual layers showed a robust representation of peripheral saliency evoked by a conspicuous stimulus embedded in a wide-field array of goal-irrelevant stimuli. In contrast, visuomotor neurons from the intermediate saccade-related layers showed a poor saliency representation, even though most of these neurons were visually responsive during smooth pursuit. These results confirm and extend previous findings that place the SCs in a unique role as a saliency map that monitors peripheral vision during foveation of stationary and now moving objects.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The saliency map has played a long-standing role in models and theories of visual attention, and it is now supported by neurobiological evidence from several cortical and subcortical brain areas. While visual saliency is computed during moments of active fixation, it is not known whether the same is true while engaged in smooth pursuit of a moving stimulus, which is very common in real-world vision. Here, we examined extrafoveal saliency coding in the superior colliculus, a midbrain area associated with attention and gaze, during smooth pursuit eye movements. We found that SC neurons from the superficial visual layers showed a robust representation of peripheral saliency evoked by a conspicuous stimulus embedded in a wide-field array of goal-irrelevant stimuli. In contrast, visuomotor neurons from the intermediate saccade-related layers showed a poor saliency representation, even though most of these neurons were visually responsive during smooth pursuit. These results confirm and extend previous findings that place the SCs in a unique role as a saliency map that monitors peripheral vision during foveation of stationary and now moving objects. |
Kael J White; Ethan S Bromberg-Martin; Sarah R Heilbronner; Kaining Zhang; Julia Pai; Suzanne N Haber; Ilya E Monosov A neural network for information seeking Journal Article Nature Communications, 10 (1), pp. 1–19, 2019. @article{White2019b, title = {A neural network for information seeking}, author = {Kael J White and Ethan S Bromberg-Martin and Sarah R Heilbronner and Kaining Zhang and Julia Pai and Suzanne N Haber and Ilya E Monosov}, doi = {10.1038/s41467-019-13135-z}, year = {2019}, date = {2019-01-01}, journal = {Nature Communications}, volume = {10}, number = {1}, pages = {1--19}, publisher = {Springer US}, abstract = {Humans and other animals often show a strong desire to know the uncertain rewards their future has in store, even when they cannot use this information to influence the outcome. However, it is unknown how the brain predicts opportunities to gain information and motivates this information-seeking behavior. Here we show that neurons in a network of interconnected subregions of primate anterior cingulate cortex and basal ganglia predict the moment of gaining information about uncertain rewards. Spontaneous increases in their information prediction signals are followed by gaze shifts toward objects associated with resolving uncertainty, and pharmacologically disrupting this network reduces the motivation to seek information. These findings demonstrate a cortico-basal ganglia mechanism responsible for motivating actions to resolve uncertainty by seeking knowledge about the future.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Humans and other animals often show a strong desire to know the uncertain rewards their future has in store, even when they cannot use this information to influence the outcome. However, it is unknown how the brain predicts opportunities to gain information and motivates this information-seeking behavior. Here we show that neurons in a network of interconnected subregions of primate anterior cingulate cortex and basal ganglia predict the moment of gaining information about uncertain rewards. Spontaneous increases in their information prediction signals are followed by gaze shifts toward objects associated with resolving uncertainty, and pharmacologically disrupting this network reduces the motivation to seek information. These findings demonstrate a cortico-basal ganglia mechanism responsible for motivating actions to resolve uncertainty by seeking knowledge about the future. |
Konstantin F Willeke; Xiaoguang Tian; Antimo Buonocore; Joachim Bellet; Araceli Ramirez-Cardenas; Ziad M Hafed Memory-guided microsaccades Journal Article Nature Communications, 10 , pp. 1–14, 2019. @article{Willeke2019, title = {Memory-guided microsaccades}, author = {Konstantin F Willeke and Xiaoguang Tian and Antimo Buonocore and Joachim Bellet and Araceli Ramirez-Cardenas and Ziad M Hafed}, doi = {10.1038/s41467-019-11711-x}, year = {2019}, date = {2019-01-01}, journal = {Nature Communications}, volume = {10}, pages = {1--14}, publisher = {Springer US}, abstract = {Despite strong evidence to the contrary in the literature, microsaccades are overwhelmingly described as involuntary eye movements. Here we show in both human subjects and monkeys that individual microsaccades of any direction can easily be triggered: (1) on demand, based on an arbitrary instruction, (2) without any special training, (3) without visual guidance by a stimulus, and (4) in a spatially and temporally accurate manner. Subjects voluntarily generated instructed “memory-guided” microsaccades readily, and similarly to how they made normal visually-guided ones. In two monkeys, we also observed midbrain superior colliculus neurons that exhibit movement-related activity bursts exclusively for memory-guided microsaccades, but not for similarly-sized visually-guided movements. Our results demonstrate behavioral and neural evidence for voluntary control over individual microsaccades, supporting recently discovered functional contributions of individual microsaccade generation to visual performance alterations and covert visual selection, as well as observations that microsaccades optimize eye position during high acuity visually-guided behavior.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Despite strong evidence to the contrary in the literature, microsaccades are overwhelmingly described as involuntary eye movements. Here we show in both human subjects and monkeys that individual microsaccades of any direction can easily be triggered: (1) on demand, based on an arbitrary instruction, (2) without any special training, (3) without visual guidance by a stimulus, and (4) in a spatially and temporally accurate manner. Subjects voluntarily generated instructed “memory-guided” microsaccades readily, and similarly to how they made normal visually-guided ones. In two monkeys, we also observed midbrain superior colliculus neurons that exhibit movement-related activity bursts exclusively for memory-guided microsaccades, but not for similarly-sized visually-guided movements. Our results demonstrate behavioral and neural evidence for voluntary control over individual microsaccades, supporting recently discovered functional contributions of individual microsaccade generation to visual performance alterations and covert visual selection, as well as observations that microsaccades optimize eye position during high acuity visually-guided behavior. |
Man Yi Yim; Xinying Cai; Xiao Jing Wang Transforming the choice outcome to an action plan in monkey lateral prefrontal cortex: A neural circuit model Journal Article Neuron, 103 , pp. 520–532, 2019. @article{Yim2019b, title = {Transforming the choice outcome to an action plan in monkey lateral prefrontal cortex: A neural circuit model}, author = {Man Yi Yim and Xinying Cai and Xiao Jing Wang}, doi = {10.1016/j.neuron.2019.05.032}, year = {2019}, date = {2019-01-01}, journal = {Neuron}, volume = {103}, pages = {520--532}, publisher = {Elsevier Inc.}, abstract = {In economic decisions, we make a good-based choice first, then we transform the outcome into an action to obtain the good. To elucidate the network mechanisms for such transformation, we constructed a neural circuit model consisting of modules representing choice, integration of choice with target locations, and the final action plan. We examined three scenarios regarding how the final action plan could emerge in the neural circuit and compared their implications with experimental data. Our model with heterogeneous connectivity predicts the coexistence of three types of neurons with distinct functions, confirmed by analyzing the neural activity in the lateral prefrontal cortex (LPFC) of behaving monkeys. We obtained a much more distinct classification of functional neuron types in the ventral than the dorsal region of LPFC, suggesting that the action plan is initially generated in ventral LPFC. Our model offers a biologically plausible neural circuit architecture that implements good-to-action transformation during economic choice.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In economic decisions, we make a good-based choice first, then we transform the outcome into an action to obtain the good. To elucidate the network mechanisms for such transformation, we constructed a neural circuit model consisting of modules representing choice, integration of choice with target locations, and the final action plan. We examined three scenarios regarding how the final action plan could emerge in the neural circuit and compared their implications with experimental data. Our model with heterogeneous connectivity predicts the coexistence of three types of neurons with distinct functions, confirmed by analyzing the neural activity in the lateral prefrontal cortex (LPFC) of behaving monkeys. We obtained a much more distinct classification of functional neuron types in the ventral than the dorsal region of LPFC, suggesting that the action plan is initially generated in ventral LPFC. Our model offers a biologically plausible neural circuit architecture that implements good-to-action transformation during economic choice. |
Andrew D Zaharia; Robbe L T Goris; Anthony J Movshon; Eero P Simoncelli Compound stimuli reveal the structure of visual motion selectivity in macaque MT neurons Journal Article eNeuro, 6 (6), pp. 1–19, 2019. @article{Zaharia2019, title = {Compound stimuli reveal the structure of visual motion selectivity in macaque MT neurons}, author = {Andrew D Zaharia and Robbe L T Goris and Anthony J Movshon and Eero P Simoncelli}, doi = {10.1523/ENEURO.0258-19.2019}, year = {2019}, date = {2019-01-01}, journal = {eNeuro}, volume = {6}, number = {6}, pages = {1--19}, abstract = {Motion selectivity in primary visual cortex (V1) is approximately separable in orientation, spatial frequency, and temporal frequency (“frequency-separable”). Models for area MT neurons posit that their selectivity arises by combining direction-selective V1 afferents whose tuning is organized around a tilted plane in the frequency domain, specifying a particular direction and speed (“velocity-separable”). This construction explains “pattern direction-selective” MT neurons, which are velocity-selective but relatively invariant to spatial structure, including spatial frequency, texture and shape. We designed a set of experiments to distinguish frequency-separable and velocity-separable models and executed them with single-unit recordings in macaque V1 and MT. Surprisingly, when tested with single drifting gratings, most MT neurons' responses are fit equally well by models with either form of separability. However, responses to plaids (sums of two moving gratings) tend to be better described as velocity-separable, especially for pattern neurons. We conclude that direction selectivity in MT is primarily computed by summing V1 afferents, but pattern-invariant velocity tuning for complex stimuli may arise from local, recurrent interactions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Motion selectivity in primary visual cortex (V1) is approximately separable in orientation, spatial frequency, and temporal frequency (“frequency-separable”). Models for area MT neurons posit that their selectivity arises by combining direction-selective V1 afferents whose tuning is organized around a tilted plane in the frequency domain, specifying a particular direction and speed (“velocity-separable”). This construction explains “pattern direction-selective” MT neurons, which are velocity-selective but relatively invariant to spatial structure, including spatial frequency, texture and shape. We designed a set of experiments to distinguish frequency-separable and velocity-separable models and executed them with single-unit recordings in macaque V1 and MT. Surprisingly, when tested with single drifting gratings, most MT neurons' responses are fit equally well by models with either form of separability. However, responses to plaids (sums of two moving gratings) tend to be better described as velocity-separable, especially for pattern neurons. We conclude that direction selectivity in MT is primarily computed by summing V1 afferents, but pattern-invariant velocity tuning for complex stimuli may arise from local, recurrent interactions. |
2018 |
Ricardo Kienitz; Joscha T Schmiedt; Katharine A Shapcott; Kleopatra Kouroupaki; Richard C Saunders; Michael Christoph Schmid Theta rhythmic neuronal activity and reaction times arising from cortical receptive field interactions during distributed attention Journal Article Current Biology, 28 (15), pp. 2377–2387, 2018. @article{Kienitz2018, title = {Theta rhythmic neuronal activity and reaction times arising from cortical receptive field interactions during distributed attention}, author = {Ricardo Kienitz and Joscha T Schmiedt and Katharine A Shapcott and Kleopatra Kouroupaki and Richard C Saunders and Michael Christoph Schmid}, doi = {10.1016/j.cub.2018.05.086}, year = {2018}, date = {2018-08-01}, journal = {Current Biology}, volume = {28}, number = {15}, pages = {2377--2387}, abstract = {Growing evidence suggests that distributed spatial attention may invoke theta (3–9 Hz) rhythmic sampling processes. The neuronal basis of such attentional sampling is, however, not fully understood. Here we show using array recordings in visual cortical area V4 of two awake macaques that presenting separate visual stimuli to the excitatory center and suppressive surround of neuronal receptive fields (RFs) elicits rhythmic multi-unit activity (MUA)at 3–6 Hz. This neuronal rhythm did not depend on small fixational eye movements. In the context of a distributed spatial attention task, during which the monkeys detected a spatially and temporally uncertain target, reaction times (RTs) exhibited similar rhythmic fluctuations. RTs were fast or slow depend-ing on the target occurrence during high or low MUA, resulting in rhythmic MUA-RT cross-correlations at theta frequencies. These findings show that theta rhythmic neuronal activity can arise from competitiveRF interactions and that this rhythm may result in rhythmic RTs potentially subserving attentional sampling.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Growing evidence suggests that distributed spatial attention may invoke theta (3–9 Hz) rhythmic sampling processes. The neuronal basis of such attentional sampling is, however, not fully understood. Here we show using array recordings in visual cortical area V4 of two awake macaques that presenting separate visual stimuli to the excitatory center and suppressive surround of neuronal receptive fields (RFs) elicits rhythmic multi-unit activity (MUA)at 3–6 Hz. This neuronal rhythm did not depend on small fixational eye movements. In the context of a distributed spatial attention task, during which the monkeys detected a spatially and temporally uncertain target, reaction times (RTs) exhibited similar rhythmic fluctuations. RTs were fast or slow depend-ing on the target occurrence during high or low MUA, resulting in rhythmic MUA-RT cross-correlations at theta frequencies. These findings show that theta rhythmic neuronal activity can arise from competitiveRF interactions and that this rhythm may result in rhythmic RTs potentially subserving attentional sampling. |
Joshua D Cosman; Kaleb A Lowe; Wolf Zinke; Geoffrey F Woodman; Jeffrey D Schall Prefrontal control of visual distraction Journal Article Current Biology, 28 (3), pp. 414–420, 2018. @article{Cosman2018, title = {Prefrontal control of visual distraction}, author = {Joshua D Cosman and Kaleb A Lowe and Wolf Zinke and Geoffrey F Woodman and Jeffrey D Schall}, doi = {10.1016/j.cub.2017.12.023}, year = {2018}, date = {2018-02-01}, journal = {Current Biology}, volume = {28}, number = {3}, pages = {414--420}, abstract = {Avoiding distraction by conspicuous but irrelevant stimuli is critical to accomplishing daily tasks. Regions of prefrontal cortex control attention by enhancing the representation of task-relevant information in sensory cortex, which can be measured in modulation of both single neurons and event-related electrical potentials (ERPs) on the cranial surface [1, 2]. When irrelevant information is particularly conspicuous, it can distract attention and interfere with the selection of behaviorally relevant information. Such distraction can be minimized via top-down control [3–5], but the cognitive and neural mechanisms giving rise to this control over distraction remain uncertain and debated [6–9]. Bridging neurophysiology to electrophysiology, we simultaneously recorded neurons in prefrontal cortex and ERPs over extrastriate visual cortex to track the processing of salient distractors during a visual search task. Critically, when the salient distractor was successfully ignored, but not otherwise, we observed robust suppression of salient distractor representations. Like target selection, the distractor suppression was observed in prefrontal cortex before it appeared over extrastriate cortical areas. Furthermore, all prefrontal neurons that showed suppression of the task-irrelevant distractor also contributed to selecting the target. This suggests a common prefrontal mechanism is responsible for both selecting task-relevant and suppressing task-irrelevant information in sensory cortex. Taken together, our results resolve a long-standing debate over the mechanisms that prevent distraction, and provide the first evidence directly linking suppressed neural firing in prefrontal cortex with surface ERP measures of distractor suppression.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Avoiding distraction by conspicuous but irrelevant stimuli is critical to accomplishing daily tasks. Regions of prefrontal cortex control attention by enhancing the representation of task-relevant information in sensory cortex, which can be measured in modulation of both single neurons and event-related electrical potentials (ERPs) on the cranial surface [1, 2]. When irrelevant information is particularly conspicuous, it can distract attention and interfere with the selection of behaviorally relevant information. Such distraction can be minimized via top-down control [3–5], but the cognitive and neural mechanisms giving rise to this control over distraction remain uncertain and debated [6–9]. Bridging neurophysiology to electrophysiology, we simultaneously recorded neurons in prefrontal cortex and ERPs over extrastriate visual cortex to track the processing of salient distractors during a visual search task. Critically, when the salient distractor was successfully ignored, but not otherwise, we observed robust suppression of salient distractor representations. Like target selection, the distractor suppression was observed in prefrontal cortex before it appeared over extrastriate cortical areas. Furthermore, all prefrontal neurons that showed suppression of the task-irrelevant distractor also contributed to selecting the target. This suggests a common prefrontal mechanism is responsible for both selecting task-relevant and suppressing task-irrelevant information in sensory cortex. Taken together, our results resolve a long-standing debate over the mechanisms that prevent distraction, and provide the first evidence directly linking suppressed neural firing in prefrontal cortex with surface ERP measures of distractor suppression. |
Amir-Mohammad Alizadeh; Ilse C Van Dromme; Peter Janssen Single-cell responses to three-dimensional structure in a functionally defined patch in macaque area TEO Journal Article Journal of Neurophysiology, 120 (6), pp. 2806–2818, 2018. @article{Alizadeh2018, title = {Single-cell responses to three-dimensional structure in a functionally defined patch in macaque area TEO}, author = {Amir-Mohammad Alizadeh and Ilse C {Van Dromme} and Peter Janssen}, doi = {10.1152/jn.00198.2018}, year = {2018}, date = {2018-01-01}, journal = {Journal of Neurophysiology}, volume = {120}, number = {6}, pages = {2806--2818}, abstract = {Both dorsal and ventral visual pathways harbor several areas sensitive to gradients of binocular disparity (i.e., higher-order disparity). Although a wealth of information exists about disparity processing in early visual (V1, V2, and V3) and end-stage areas, TE in the ventral stream, and the anterior intraparietal area (AIP) in the dorsal stream, little is known about midlevel area TEO in the ventral pathway. We recorded single-unit responses to disparity-defined curved stimuli in a functional magnetic resonance imaging (fMRI) activation elicited by curved surfaces compared with flat surfaces in the macaque area TEO. This fMRI activation contained a small proportion of disparity- selective neurons, with very few of them second-order disparity selective. Overall, this population of TEO neurons did not preserve its three-dimensional structure selectivity across positions in depth, in- dicating a lack of higher-order disparity selectivity, but showed stronger responses to flat surfaces than to curved surfaces, as predicted by the fMRI experiment. The receptive fields of the responsive TEO cells were relatively small and generally foveal. A linear support vector machine classifier showed that this population of disparity-selective TEO neurons contains reliable information about the sign of curvature and the position in depth of the stimulus.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Both dorsal and ventral visual pathways harbor several areas sensitive to gradients of binocular disparity (i.e., higher-order disparity). Although a wealth of information exists about disparity processing in early visual (V1, V2, and V3) and end-stage areas, TE in the ventral stream, and the anterior intraparietal area (AIP) in the dorsal stream, little is known about midlevel area TEO in the ventral pathway. We recorded single-unit responses to disparity-defined curved stimuli in a functional magnetic resonance imaging (fMRI) activation elicited by curved surfaces compared with flat surfaces in the macaque area TEO. This fMRI activation contained a small proportion of disparity- selective neurons, with very few of them second-order disparity selective. Overall, this population of TEO neurons did not preserve its three-dimensional structure selectivity across positions in depth, in- dicating a lack of higher-order disparity selectivity, but showed stronger responses to flat surfaces than to curved surfaces, as predicted by the fMRI experiment. The receptive fields of the responsive TEO cells were relatively small and generally foveal. A linear support vector machine classifier showed that this population of disparity-selective TEO neurons contains reliable information about the sign of curvature and the position in depth of the stimulus. |
Amir-Mohammad Alizadeh; Ilse Van Dromme; Bram-Ernst Verhoef; Peter Janssen Caudal Intraparietal Sulcus and three-dimensional vision: A combined functional magnetic resonance imaging and single-cell study Journal Article NeuroImage, 166 , pp. 46–59, 2018. @article{Alizadeh2018a, title = {Caudal Intraparietal Sulcus and three-dimensional vision: A combined functional magnetic resonance imaging and single-cell study}, author = {Amir-Mohammad Alizadeh and Ilse {Van Dromme} and Bram-Ernst Verhoef and Peter Janssen}, doi = {10.1016/j.neuroimage.2017.10.045}, year = {2018}, date = {2018-01-01}, journal = {NeuroImage}, volume = {166}, pages = {46--59}, publisher = {Elsevier Ltd}, abstract = {The cortical network processing three-dimensional (3D) object structure defined by binocular disparity spans both the ventral and dorsal visual streams. However, very little is known about the neural representation of 3D structure at intermediate levels of the visual hierarchy. Here, we investigated the neural selectivity for 3D surfaces in the macaque Posterior Intraparietal area (PIP) in the medial bank of the caudal intraparietal sulcus (IPS). We first identified a region sensitive to depth-structure information in the medial bank of the caudal IPS using functional Magnetic Resonance Imaging (fMRI), and then recorded single-cell activity within this fMRI activation in the same animals. Most PIP neurons were selective for the 3D orientation of planar surfaces (first-order disparity) at very short latencies, whereas a very small fraction of PIP neurons were selective for curved surfaces (second-order disparity). A linear support vector machine classifier could reliably identify the direction of the disparity gradient in planar and curved surfaces based on the responses of a population of disparity-selective PIP neurons. These results provide the first detailed account of the neuronal properties in area PIP, which occupies an intermediate position in the hierarchy of visual areas involved in processing depth structure from disparity.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The cortical network processing three-dimensional (3D) object structure defined by binocular disparity spans both the ventral and dorsal visual streams. However, very little is known about the neural representation of 3D structure at intermediate levels of the visual hierarchy. Here, we investigated the neural selectivity for 3D surfaces in the macaque Posterior Intraparietal area (PIP) in the medial bank of the caudal intraparietal sulcus (IPS). We first identified a region sensitive to depth-structure information in the medial bank of the caudal IPS using functional Magnetic Resonance Imaging (fMRI), and then recorded single-cell activity within this fMRI activation in the same animals. Most PIP neurons were selective for the 3D orientation of planar surfaces (first-order disparity) at very short latencies, whereas a very small fraction of PIP neurons were selective for curved surfaces (second-order disparity). A linear support vector machine classifier could reliably identify the direction of the disparity gradient in planar and curved surfaces based on the responses of a population of disparity-selective PIP neurons. These results provide the first detailed account of the neuronal properties in area PIP, which occupies an intermediate position in the hierarchy of visual areas involved in processing depth structure from disparity. |
Ken ichi Amemori; Satoko Amemori; Daniel J Gibson; Ann M Graybiel Striatal microstimulation induces persistent and repetitive negative decision-making predicted by striatal beta-band oscillation Journal Article Neuron, 99 (4), pp. 829–841, 2018. @article{Amemori2018, title = {Striatal microstimulation induces persistent and repetitive negative decision-making predicted by striatal beta-band oscillation}, author = {Ken ichi Amemori and Satoko Amemori and Daniel J Gibson and Ann M Graybiel}, doi = {10.1016/j.neuron.2018.07.022}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {99}, number = {4}, pages = {829--841}, publisher = {Elsevier Inc.}, abstract = {Persistent thoughts inducing irrationally pessimistic and repetitive decisions are often symptoms of mood and anxiety disorders. Regional neural hyper-activities have been associated with these disorders, but it remains unclear whether there is a specific brain region causally involved in these persistent valuations. Here, we identified potential sources of such persistent states by microstimulating the striatum of macaques performing a task by which we could quantitatively estimate their subjective pessimistic states using their choices to accept or reject conflicting offers. We found that this microstimulation induced irrationally repetitive choices with negative evaluations. Local field potentials recorded in the same microstimulation sessions exhibited modulations of beta-band oscillatory activity that paralleled the persistent negative states influencing repetitive decisions. These findings demonstrate that local striatal zones can causally affect subjective states influencing persistent negative valuation and that abnormal beta-band oscillations can be associated with persistency in valuation accompanied by an anxiety-like state.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Persistent thoughts inducing irrationally pessimistic and repetitive decisions are often symptoms of mood and anxiety disorders. Regional neural hyper-activities have been associated with these disorders, but it remains unclear whether there is a specific brain region causally involved in these persistent valuations. Here, we identified potential sources of such persistent states by microstimulating the striatum of macaques performing a task by which we could quantitatively estimate their subjective pessimistic states using their choices to accept or reject conflicting offers. We found that this microstimulation induced irrationally repetitive choices with negative evaluations. Local field potentials recorded in the same microstimulation sessions exhibited modulations of beta-band oscillatory activity that paralleled the persistent negative states influencing repetitive decisions. These findings demonstrate that local striatal zones can causally affect subjective states influencing persistent negative valuation and that abnormal beta-band oscillations can be associated with persistency in valuation accompanied by an anxiety-like state. |
Fabrice Arcizet; Richard J Krauzlis Covert spatial selection in primate basal ganglia Journal Article PLoS Biology, 16 (10), pp. 1–28, 2018. @article{Arcizet2018, title = {Covert spatial selection in primate basal ganglia}, author = {Fabrice Arcizet and Richard J Krauzlis}, doi = {10.1371/journal.pbio.2005930}, year = {2018}, date = {2018-01-01}, journal = {PLoS Biology}, volume = {16}, number = {10}, pages = {1--28}, abstract = {The basal ganglia are important for action selection. They are also implicated in perceptual and cognitive functions that seem far removed from motor control. Here, we tested whether the role of the basal ganglia in selection extends to nonmotor aspects of behavior by recording neuronal activity in the caudate nucleus while animals performed a covert spatial attention task. We found that caudate neurons strongly select the spatial location of the relevant stimulus throughout the task even in the absence of any overt action. This spatially selective activity was dependent on task and visual conditions and could be dissociated from goal-directed actions. Caudate activity was also sufficient to correctly identify every epoch in the covert attention task. These results provide a novel perspective on mechanisms of attention by demonstrating that the basal ganglia are involved in spatial selection and tracking of behavioral states even in the absence of overt orienting movements.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The basal ganglia are important for action selection. They are also implicated in perceptual and cognitive functions that seem far removed from motor control. Here, we tested whether the role of the basal ganglia in selection extends to nonmotor aspects of behavior by recording neuronal activity in the caudate nucleus while animals performed a covert spatial attention task. We found that caudate neurons strongly select the spatial location of the relevant stimulus throughout the task even in the absence of any overt action. This spatially selective activity was dependent on task and visual conditions and could be dissociated from goal-directed actions. Caudate activity was also sufficient to correctly identify every epoch in the covert attention task. These results provide a novel perspective on mechanisms of attention by demonstrating that the basal ganglia are involved in spatial selection and tracking of behavioral states even in the absence of overt orienting movements. |
Habiba Azab; Benjamin Y Hayden Correlates of economic decisions in the dorsal and subgenual anterior cingulate cortices Journal Article European Journal of Neuroscience, 47 (8), pp. 979–993, 2018. @article{Azab2018, title = {Correlates of economic decisions in the dorsal and subgenual anterior cingulate cortices}, author = {Habiba Azab and Benjamin Y Hayden}, doi = {10.1111/ejn.13865}, year = {2018}, date = {2018-01-01}, journal = {European Journal of Neuroscience}, volume = {47}, number = {8}, pages = {979--993}, abstract = {The anterior cingulate cortex can be divided into distinct ventral (subgenual, sgACC) and dorsal (dACC), portions. The role of dACC in value-based decision-making is hotly debated, while the role of sgACC is poorly understood. We recorded neuronal activity in both regions in rhesus macaques performing a token-gambling task. We find that both encode many of the same vari- ables; including integrated offered values of gambles, primary as well as secondary reward outcomes, number of current tokens and anticipated rewards. Both regions exhibit memory traces for offer values and putative value comparison signals. Both regions use a consistent scheme to encode the value of the attended option. This result suggests that neurones do not appear to be spe- cialized for specific offers (that is, neurones use an attentional as opposed to labelled line coding scheme). We also observed some differences between the two regions: (i) coding strengths in dACC were consistently greater than those in sgACC, (ii) neu- rones in sgACC responded especially to losses and in anticipation of primary rewards, while those in dACC showed more bal- anced responding and (iii) responses to the first offer were slightly faster in sgACC. These results indicate that sgACC and dACC have some functional overlap in economic choice, and are consistent with the idea, inspired by neuroanatomy, which sgACC may serve as input to dACC.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The anterior cingulate cortex can be divided into distinct ventral (subgenual, sgACC) and dorsal (dACC), portions. The role of dACC in value-based decision-making is hotly debated, while the role of sgACC is poorly understood. We recorded neuronal activity in both regions in rhesus macaques performing a token-gambling task. We find that both encode many of the same vari- ables; including integrated offered values of gambles, primary as well as secondary reward outcomes, number of current tokens and anticipated rewards. Both regions exhibit memory traces for offer values and putative value comparison signals. Both regions use a consistent scheme to encode the value of the attended option. This result suggests that neurones do not appear to be spe- cialized for specific offers (that is, neurones use an attentional as opposed to labelled line coding scheme). We also observed some differences between the two regions: (i) coding strengths in dACC were consistently greater than those in sgACC, (ii) neu- rones in sgACC responded especially to losses and in anticipation of primary rewards, while those in dACC showed more bal- anced responding and (iii) responses to the first offer were slightly faster in sgACC. These results indicate that sgACC and dACC have some functional overlap in economic choice, and are consistent with the idea, inspired by neuroanatomy, which sgACC may serve as input to dACC. |
Theda Backen; Stefan Treue; Julio C Martinez-Trujillo Encoding of spatial attention by primate prefrontal cortex neuronal ensembles Journal Article Eneuro, 5 (1), pp. 1–19, 2018. @article{Backen2018, title = {Encoding of spatial attention by primate prefrontal cortex neuronal ensembles}, author = {Theda Backen and Stefan Treue and Julio C Martinez-Trujillo}, doi = {10.1523/eneuro.0372-16.2017}, year = {2018}, date = {2018-01-01}, journal = {Eneuro}, volume = {5}, number = {1}, pages = {1--19}, abstract = {Single neurons in the primate lateral prefrontal cortex (LPFC) encode information about the allocation of visual attention and the features of visual stimuli. However, how this compares to the performance of neuronal ensembles at encoding the same information is poorly understood. Here, we recorded the responses of neuronal ensembles in the LPFC of two macaque monkeys while they performed a task that required attending to one of two moving random dot patterns positioned in different hemifields and ignoring the other pattern. We found single units selective for the location of the attended stimulus as well as for its motion direction. To determine the coding of both variables in the population of recorded units, we used a linear classifier and progressively built neuronal ensembles by iteratively adding units according to their individual performance (best single units), or by iteratively adding units based on their contribution to the ensemble performance (best ensemble). For both methods, ensembles of relatively small sizes (n textless 60) yielded substantially higher decoding performance relative to individual single units. However, the decoder reached similar performance using fewer neurons with the best ensemble building method compared to the best single units method. Our results indicate that neuronal ensembles within the LPFC encode more information about the attended spatial and non-spatial features of visual stimuli than individual neurons. They further suggest that efficient coding of attention can be achieved by relatively small neuronal ensembles characterized by a certain relationship between signal and noise correlation structures. Significance Statement Single neurons in the primate lateral prefrontal cortex (LPFC) are known to encode the spatial location of attended stimuli as well as other visual features. Here, we investigate how these single neuron coding properties translate into how ensembles of neurons encode information. Our results show that LPFC neuronal ensembles encode both the allocation of attention and the direction of motion of moving stimuli with higher efficiency than single units. Furthermore, relatively small ensembles reach the same decoding accuracy as the full ensembles. Our findings indicate that information coding by neuronal ensembles within the LPFC depends on complex network properties that cannot be solely estimated from coding properties of individual neurons.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Single neurons in the primate lateral prefrontal cortex (LPFC) encode information about the allocation of visual attention and the features of visual stimuli. However, how this compares to the performance of neuronal ensembles at encoding the same information is poorly understood. Here, we recorded the responses of neuronal ensembles in the LPFC of two macaque monkeys while they performed a task that required attending to one of two moving random dot patterns positioned in different hemifields and ignoring the other pattern. We found single units selective for the location of the attended stimulus as well as for its motion direction. To determine the coding of both variables in the population of recorded units, we used a linear classifier and progressively built neuronal ensembles by iteratively adding units according to their individual performance (best single units), or by iteratively adding units based on their contribution to the ensemble performance (best ensemble). For both methods, ensembles of relatively small sizes (n textless 60) yielded substantially higher decoding performance relative to individual single units. However, the decoder reached similar performance using fewer neurons with the best ensemble building method compared to the best single units method. Our results indicate that neuronal ensembles within the LPFC encode more information about the attended spatial and non-spatial features of visual stimuli than individual neurons. They further suggest that efficient coding of attention can be achieved by relatively small neuronal ensembles characterized by a certain relationship between signal and noise correlation structures. Significance Statement Single neurons in the primate lateral prefrontal cortex (LPFC) are known to encode the spatial location of attended stimuli as well as other visual features. Here, we investigate how these single neuron coding properties translate into how ensembles of neurons encode information. Our results show that LPFC neuronal ensembles encode both the allocation of attention and the direction of motion of moving stimuli with higher efficiency than single units. Furthermore, relatively small ensembles reach the same decoding accuracy as the full ensembles. Our findings indicate that information coding by neuronal ensembles within the LPFC depends on complex network properties that cannot be solely estimated from coding properties of individual neurons. |
Zahra Bahmani; Mohammad Reza Daliri; Yaser Merrikhi; Kelsey Clark; Behrad Noudoost Working memory enhances cortical representations via spatially specific coordination of spike times Journal Article Neuron, 97 (4), pp. 967–979, 2018. @article{Bahmani2018, title = {Working memory enhances cortical representations via spatially specific coordination of spike times}, author = {Zahra Bahmani and Mohammad Reza Daliri and Yaser Merrikhi and Kelsey Clark and Behrad Noudoost}, doi = {10.1016/j.neuron.2018.01.012}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {97}, number = {4}, pages = {967--979}, publisher = {Elsevier Inc.}, abstract = {The online maintenance and manipulation of information in working memory (WM) is essential for guiding behavior based on our goals. Understanding how WM alters sensory processing in pursuit of different behavioral objectives is therefore crucial to establish the neural basis of our goal-directed behavior. Here we show that, in the middle temporal (MT) area of rhesus monkeys, the power of the local field potentials in the ab band (8–25 Hz) increases, reflecting the remembered location and the animal's performance. Moreover, the content of WM determines how coherently MT sites oscillate and how synchronized spikes are relative to these oscillations. These changes in spike timing are not only sufficient to carry sensory and memory information, they can also account for WM-induced sensory enhancement. These results provide a mechanistic-level understanding of how WM alters sensory processing by coordinating the timing of spikes across the neuronal population, enhancing the sensory representation of WM targets.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The online maintenance and manipulation of information in working memory (WM) is essential for guiding behavior based on our goals. Understanding how WM alters sensory processing in pursuit of different behavioral objectives is therefore crucial to establish the neural basis of our goal-directed behavior. Here we show that, in the middle temporal (MT) area of rhesus monkeys, the power of the local field potentials in the ab band (8–25 Hz) increases, reflecting the remembered location and the animal's performance. Moreover, the content of WM determines how coherently MT sites oscillate and how synchronized spikes are relative to these oscillations. These changes in spike timing are not only sufficient to carry sensory and memory information, they can also account for WM-induced sensory enhancement. These results provide a mechanistic-level understanding of how WM alters sensory processing by coordinating the timing of spikes across the neuronal population, enhancing the sensory representation of WM targets. |
Giacomo Benvenuti; Yuzhi Chen; Charu Ramakrishnan; Karl Deisseroth; Wilson S Geisler; Eyal Seidemann Scale-invariant visual capabilities explained by topographic representations of luminance and texture in primate V1 Journal Article Neuron, 100 (6), pp. 1504–1512., 2018. @article{Benvenuti2018, title = {Scale-invariant visual capabilities explained by topographic representations of luminance and texture in primate V1}, author = {Giacomo Benvenuti and Yuzhi Chen and Charu Ramakrishnan and Karl Deisseroth and Wilson S Geisler and Eyal Seidemann}, doi = {10.1016/j.neuron.2018.10.020}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {100}, number = {6}, pages = {1504--1512.}, publisher = {Elsevier}, abstract = {Humans have remarkable scale-invariant visual capabilities. For example, our orientation discrimination sensitivity is largely constant over more than two orders of magnitude of variations in stimulus spatial frequency (SF). Orientation-selective V1 neurons are likely to contribute to orientation discrimination. However, because at any V1 location neurons have a limited range of receptive field (RF) sizes, we predict that at low SFs V1 neurons will carry little orientation information. If this were the case, what could account for the high behavioral sensitivity at low SFs? Using optical imaging in behaving macaques, we show that, as predicted, V1 orientation-tuned responses drop rapidly with decreasing SF. However, we reveal a surprising coarse-scale signal that corresponds to the projection of the luminance layout of low-SF stimuli to V1's retinotopic map. This homeomorphic and distributed representation, which carries high-quality orientation information, is likely to contribute to our striking scale-invariant visual capabilities.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Humans have remarkable scale-invariant visual capabilities. For example, our orientation discrimination sensitivity is largely constant over more than two orders of magnitude of variations in stimulus spatial frequency (SF). Orientation-selective V1 neurons are likely to contribute to orientation discrimination. However, because at any V1 location neurons have a limited range of receptive field (RF) sizes, we predict that at low SFs V1 neurons will carry little orientation information. If this were the case, what could account for the high behavioral sensitivity at low SFs? Using optical imaging in behaving macaques, we show that, as predicted, V1 orientation-tuned responses drop rapidly with decreasing SF. However, we reveal a surprising coarse-scale signal that corresponds to the projection of the luminance layout of low-SF stimuli to V1's retinotopic map. This homeomorphic and distributed representation, which carries high-quality orientation information, is likely to contribute to our striking scale-invariant visual capabilities. |
Anil Bollimunta; Amarender R Bogadhi; Richard J Krauzlis Comparing frontal eye field and superior colliculus contributions to covert spatial attention Journal Article Nature Communications, 9 , pp. 1–11, 2018. @article{Bollimunta2018, title = {Comparing frontal eye field and superior colliculus contributions to covert spatial attention}, author = {Anil Bollimunta and Amarender R Bogadhi and Richard J Krauzlis}, doi = {10.1038/s41467-018-06042-2}, year = {2018}, date = {2018-01-01}, journal = {Nature Communications}, volume = {9}, pages = {1--11}, abstract = {The causal roles of the frontal eye fields (FEF) and superior colliculus (SC) in spatial selective attention have not been directly compared. Reversible inactivation is an established method for testing causality but comparing results between FEF and SC is complicated by differences in size and morphology of the two brain regions. Here we exploited the fact that inactivation of FEF and SC also changes the metrics of saccadic eye movements, providing an independent benchmark for the strength of the causal manipulation. Using monkeys trained to covertly perform a visual motion-change detection task, we found that inactivation of either FEF or SC could cause deficits in attention task performance. However, SC-induced attention deficits were found with saccade changes half the size needed to get FEF-induced attention deficits. Thus, performance in visual attention tasks is vulnerable to loss of signals from either structure, but suppression of SC activity has a more devastating effect.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The causal roles of the frontal eye fields (FEF) and superior colliculus (SC) in spatial selective attention have not been directly compared. Reversible inactivation is an established method for testing causality but comparing results between FEF and SC is complicated by differences in size and morphology of the two brain regions. Here we exploited the fact that inactivation of FEF and SC also changes the metrics of saccadic eye movements, providing an independent benchmark for the strength of the causal manipulation. Using monkeys trained to covertly perform a visual motion-change detection task, we found that inactivation of either FEF or SC could cause deficits in attention task performance. However, SC-induced attention deficits were found with saccade changes half the size needed to get FEF-induced attention deficits. Thus, performance in visual attention tasks is vulnerable to loss of signals from either structure, but suppression of SC activity has a more devastating effect. |
Yehudit Botschko; Merav Yarkoni; Mati Joshua Smooth pursuit eye movement of monkeys naive to laboratory setups with pictures and artificial stimuli Journal Article Frontiers in Systems Neuroscience, 12 , pp. 1–11, 2018. @article{Botschko2018, title = {Smooth pursuit eye movement of monkeys naive to laboratory setups with pictures and artificial stimuli}, author = {Yehudit Botschko and Merav Yarkoni and Mati Joshua}, doi = {10.3389/fnsys.2018.00015}, year = {2018}, date = {2018-01-01}, journal = {Frontiers in Systems Neuroscience}, volume = {12}, pages = {1--11}, abstract = {When animal behavior is studied in a laboratory environment, the animals are often extensively trained to shape their behavior. A crucial question is whether the behavior observed after training is part of the natural repertoire of the animal or represents an outlier in the animal's natural capabilities. This can be investigated by assessing the extent to which the target behavior is manifested during the initial stages of training and the time course of learning. We explored this issue by examining smooth pursuit eye movements in monkeys naïve to smooth pursuit tasks. We recorded the eye movements of monkeys from the first days of training on a step-ramp paradigm. We used bright spots, monkey pictures and scrambled versions of the pictures as moving targets. We found that during the initial stages of training, the pursuit initiation was largest for the monkey pictures and in some direction conditions close to target velocity. When the pursuit initiation was large, the monkeys mostly continued to track the target with smooth pursuit movements while correcting for displacement errors with small saccades. Two weeks of training increased the pursuit eye velocity in all stimulus conditions, whereas further extensive training enhanced pursuit slightly more. The training decreased the coefficient of variation of the eye velocity. Anisotropies that grade pursuit across directions were observed from the first day of training and mostly persisted across training. Thus, smooth pursuit in the step-ramp paradigm appears to be part of the natural repertoire of monkeys' behavior and training adjusts monkeys' natural predisposed behavior.}, keywords = {}, pubstate = {published}, tppubtype = {article} } When animal behavior is studied in a laboratory environment, the animals are often extensively trained to shape their behavior. A crucial question is whether the behavior observed after training is part of the natural repertoire of the animal or represents an outlier in the animal's natural capabilities. This can be investigated by assessing the extent to which the target behavior is manifested during the initial stages of training and the time course of learning. We explored this issue by examining smooth pursuit eye movements in monkeys naïve to smooth pursuit tasks. We recorded the eye movements of monkeys from the first days of training on a step-ramp paradigm. We used bright spots, monkey pictures and scrambled versions of the pictures as moving targets. We found that during the initial stages of training, the pursuit initiation was largest for the monkey pictures and in some direction conditions close to target velocity. When the pursuit initiation was large, the monkeys mostly continued to track the target with smooth pursuit movements while correcting for displacement errors with small saccades. Two weeks of training increased the pursuit eye velocity in all stimulus conditions, whereas further extensive training enhanced pursuit slightly more. The training decreased the coefficient of variation of the eye velocity. Anisotropies that grade pursuit across directions were observed from the first day of training and mostly persisted across training. Thus, smooth pursuit in the step-ramp paradigm appears to be part of the natural repertoire of monkeys' behavior and training adjusts monkeys' natural predisposed behavior. |
Irene Caprara; Peter Janssen; Maria C Romero Investigating object representations in the macaque dorsal visual stream using single-unit recordings Journal Article Journal of Visualized Experiments, (138), pp. 1–10, 2018. @article{Caprara2018a, title = {Investigating object representations in the macaque dorsal visual stream using single-unit recordings}, author = {Irene Caprara and Peter Janssen and Maria C Romero}, doi = {10.3791/57745}, year = {2018}, date = {2018-01-01}, journal = {Journal of Visualized Experiments}, number = {138}, pages = {1--10}, abstract = {Previous studies have shown that neurons in parieto-frontal areas of the macaque brain can be highly selective for real-world objects, disparity-defined curved surfaces, and images of real-world objects (with and without disparity) in a similar manner as described in the ventral visual stream. In addition, parieto-frontal areas are believed to convert visual object information into appropriate motor outputs, such as the pre-shaping of the hand during grasping. To better characterize object selectivity in the cortical network involved in visuomotor transformations, we provide a battery of tests intended to analyze the visual object selectivity of neurons in parieto-frontal regions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Previous studies have shown that neurons in parieto-frontal areas of the macaque brain can be highly selective for real-world objects, disparity-defined curved surfaces, and images of real-world objects (with and without disparity) in a similar manner as described in the ventral visual stream. In addition, parieto-frontal areas are believed to convert visual object information into appropriate motor outputs, such as the pre-shaping of the hand during grasping. To better characterize object selectivity in the cortical network involved in visuomotor transformations, we provide a battery of tests intended to analyze the visual object selectivity of neurons in parieto-frontal regions. |
Irene Caprara; Elsie Premereur; Maria C Romero; Pedro Faria; Peter Janssen Shape responses in a macaque frontal area connected to posterior parietal cortex Journal Article NeuroImage, 179 , pp. 298–312, 2018. @article{Caprara2018b, title = {Shape responses in a macaque frontal area connected to posterior parietal cortex}, author = {Irene Caprara and Elsie Premereur and Maria C Romero and Pedro Faria and Peter Janssen}, doi = {10.1016/j.neuroimage.2018.06.052}, year = {2018}, date = {2018-01-01}, journal = {NeuroImage}, volume = {179}, pages = {298--312}, publisher = {Elsevier Ltd}, abstract = {The primate dorsal visual stream processes object shape to guide actions involving an object, but the transmission of shape information beyond posterior parietal cortex remains largely unknown. To clarify the information flow between parietal and frontal cortex, we applied electrical microstimulation during functional Magnetic Resonance Imaging (fMRI) in a shape-selective patch in the posterior part of the Anterior Intraparietal area (pAIP) to chart its connectivity. Subsequently, we recorded single-unit responses to images of objects in the fMRI activation in prefrontal cortex, corresponding to area 45B, elicited by pAIP microstimulation. Neurons in area 45B had properties similar to neurons in pAIP, responding selectively to shape contours and to very small shape fragments measuring less than one deg at exceedingly short latencies. However, contrary to the prevailing view on the hierarchical organization of cortical areas, neurons in area 45B preferred even smaller shape fragments and had smaller receptive fields than neurons in pAIP. These findings provide the first evidence for ultra-fast shape processing in prefrontal cortex, and suggest that the pathway from pAIP to area 45B may not be important for object grasping.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The primate dorsal visual stream processes object shape to guide actions involving an object, but the transmission of shape information beyond posterior parietal cortex remains largely unknown. To clarify the information flow between parietal and frontal cortex, we applied electrical microstimulation during functional Magnetic Resonance Imaging (fMRI) in a shape-selective patch in the posterior part of the Anterior Intraparietal area (pAIP) to chart its connectivity. Subsequently, we recorded single-unit responses to images of objects in the fMRI activation in prefrontal cortex, corresponding to area 45B, elicited by pAIP microstimulation. Neurons in area 45B had properties similar to neurons in pAIP, responding selectively to shape contours and to very small shape fragments measuring less than one deg at exceedingly short latencies. However, contrary to the prevailing view on the hierarchical organization of cortical areas, neurons in area 45B preferred even smaller shape fragments and had smaller receptive fields than neurons in pAIP. These findings provide the first evidence for ultra-fast shape processing in prefrontal cortex, and suggest that the pathway from pAIP to area 45B may not be important for object grasping. |
Chih Yang Chen; Lukas Sonnenberg; Simone Weller; Thede Witschel; Ziad M Hafed Spatial frequency sensitivity in macaque midbrain Journal Article Nature Communications, 9 (1), pp. 1–13, 2018. @article{Chen2018c, title = {Spatial frequency sensitivity in macaque midbrain}, author = {Chih Yang Chen and Lukas Sonnenberg and Simone Weller and Thede Witschel and Ziad M Hafed}, doi = {10.1038/s41467-018-05302-5}, year = {2018}, date = {2018-01-01}, journal = {Nature Communications}, volume = {9}, number = {1}, pages = {1--13}, publisher = {Springer US}, abstract = {Visual brain areas exhibit tuning characteristics well suited for image statistics present in our natural environment. However, visual sensation is an active process, and if there are any brain areas that ought to be particularly in tune with natural scene statistics, it would be sensory-motor areas critical for guiding behavior. Here we found that the rhesus macaque superior colliculus, a structure instrumental for rapid visual exploration with saccades, detects low spatial frequencies, which are the most prevalent in natural scenes, much more rapidly than high spatial frequencies. Importantly, this accelerated detection happens independently of whether a neuron is more or less sensitive to low spatial frequencies to begin with. At the population level, the superior colliculus additionally over-represents low spatial frequencies in neural response sensitivity, even at near-foveal eccentricities. Thus, the superior colliculus possesses both temporal and response gain mechanisms for efficient gaze realignment in low-spatial-frequency-dominated natural environments.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual brain areas exhibit tuning characteristics well suited for image statistics present in our natural environment. However, visual sensation is an active process, and if there are any brain areas that ought to be particularly in tune with natural scene statistics, it would be sensory-motor areas critical for guiding behavior. Here we found that the rhesus macaque superior colliculus, a structure instrumental for rapid visual exploration with saccades, detects low spatial frequencies, which are the most prevalent in natural scenes, much more rapidly than high spatial frequencies. Importantly, this accelerated detection happens independently of whether a neuron is more or less sensitive to low spatial frequencies to begin with. At the population level, the superior colliculus additionally over-represents low spatial frequencies in neural response sensitivity, even at near-foveal eccentricities. Thus, the superior colliculus possesses both temporal and response gain mechanisms for efficient gaze realignment in low-spatial-frequency-dominated natural environments. |
Hoseok Choi; Seho Lee; Jeyeon Lee; Kyeongran Min; Seokbeen Lim; Jinsick Park; Kyoung ha Ahn; In Young Kim; Kyoung-Min Lee; Dong Pyo Jang Long-term evaluation and feasibility study of the insulated screw electrode for ECoG recording Journal Article Journal of Neuroscience Methods, 308 , pp. 261–268, 2018. @article{Choi2018, title = {Long-term evaluation and feasibility study of the insulated screw electrode for ECoG recording}, author = {Hoseok Choi and Seho Lee and Jeyeon Lee and Kyeongran Min and Seokbeen Lim and Jinsick Park and Kyoung ha Ahn and In Young Kim and Kyoung-Min Lee and Dong Pyo Jang}, doi = {10.1016/j.jneumeth.2018.06.027}, year = {2018}, date = {2018-01-01}, journal = {Journal of Neuroscience Methods}, volume = {308}, pages = {261--268}, publisher = {Elsevier}, abstract = {Background: A screw-shaped electrode can offer a compromise between signal quality and invasiveness. However, the standard screw electrode can be vulnerable to electrical noise while directly contact with the skull or skin, and the feasibility and stability for chronic implantation in primate have not been fully evaluated. New Method: We designed a novel screw electrocorticogram (ECoG) electrode composed of three parts: recording electrode, insulator, and nut. The recording electrode was made of titanium with high biocompatibility and high electrical conductivity. Zirconia is used for insulator and nut to prevent electrical noise. Result: In computer simulations, the screw ECoG with insulator showed a significantly higher performance in signal acquisition compared to the condition without insulator. In a non-human primate, using screw ECoG, clear visual-evoked potential (VEP) waveforms were obtained, VEP components were reliably maintained, and the electrode's impedance was stable during the whole evaluation period. Moreover, it showed higher SNR and wider frequency band compared to the electroencephalogram (EEG). We also observed the screw ECoG has a higher sensitivity that captures different responses on various stimuli than the EEG. Comparison: The screw ECoG showed reliable electrical characteristic and biocompatibility for three months, that shows great promise for chronic implants. These results contrasted with previous reports that general screw electrode was only applicable for acute applications. Conclusion: The suggested electrode can offer whole-brain monitoring with high signal quality and minimal invasiveness. The screw ECoG can be used to provide more in-depth understanding, not only relationship between functional networks and cognitive behavior, but also pathomechanisms in brain diseases.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Background: A screw-shaped electrode can offer a compromise between signal quality and invasiveness. However, the standard screw electrode can be vulnerable to electrical noise while directly contact with the skull or skin, and the feasibility and stability for chronic implantation in primate have not been fully evaluated. New Method: We designed a novel screw electrocorticogram (ECoG) electrode composed of three parts: recording electrode, insulator, and nut. The recording electrode was made of titanium with high biocompatibility and high electrical conductivity. Zirconia is used for insulator and nut to prevent electrical noise. Result: In computer simulations, the screw ECoG with insulator showed a significantly higher performance in signal acquisition compared to the condition without insulator. In a non-human primate, using screw ECoG, clear visual-evoked potential (VEP) waveforms were obtained, VEP components were reliably maintained, and the electrode's impedance was stable during the whole evaluation period. Moreover, it showed higher SNR and wider frequency band compared to the electroencephalogram (EEG). We also observed the screw ECoG has a higher sensitivity that captures different responses on various stimuli than the EEG. Comparison: The screw ECoG showed reliable electrical characteristic and biocompatibility for three months, that shows great promise for chronic implants. These results contrasted with previous reports that general screw electrode was only applicable for acute applications. Conclusion: The suggested electrode can offer whole-brain monitoring with high signal quality and minimal invasiveness. The screw ECoG can be used to provide more in-depth understanding, not only relationship between functional networks and cognitive behavior, but also pathomechanisms in brain diseases. |
Jan Churan; Doris I Braun; Karl R Gegenfurtner; Frank Bremmer Comparison of the precision of smooth pursuit in humans and head unrestrained monkeys Journal Article Journal of Eye Movement Research, 11 (4), pp. 1–15, 2018. @article{Churan2018, title = {Comparison of the precision of smooth pursuit in humans and head unrestrained monkeys}, author = {Jan Churan and Doris I Braun and Karl R Gegenfurtner and Frank Bremmer}, doi = {10.16910/JEMR.11.4.6}, year = {2018}, date = {2018-01-01}, journal = {Journal of Eye Movement Research}, volume = {11}, number = {4}, pages = {1--15}, abstract = {Direct comparison of results of humans and monkeys is often complicated by differences in experimental conditions. We replicated in head unrestrained macaques experiments of a recent study comparing human directional precision during smooth pursuit eye movements (SPEM) and saccades to moving targets (Braun & Gegenfurtner, 2016). Directional precision of human SPEM follows an exponential decay function reaching optimal values of 1.5°-3° within 300 ms after target motion onset, whereas precision of initial saccades to moving targets is slightly better. As in humans, we found general agreement in the development of directional precision of SPEM over time and in the differences between directional precision of initial saccades and SPEM initiation. However, monkeys showed overall lower precision in SPEM compared to humans. This was most likely due to differences in experimental conditions, such as in the stabilization of the head, which was by a chin and a head rest in human subjects and unrestrained in monkeys.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Direct comparison of results of humans and monkeys is often complicated by differences in experimental conditions. We replicated in head unrestrained macaques experiments of a recent study comparing human directional precision during smooth pursuit eye movements (SPEM) and saccades to moving targets (Braun & Gegenfurtner, 2016). Directional precision of human SPEM follows an exponential decay function reaching optimal values of 1.5°-3° within 300 ms after target motion onset, whereas precision of initial saccades to moving targets is slightly better. As in humans, we found general agreement in the development of directional precision of SPEM over time and in the differences between directional precision of initial saccades and SPEM initiation. However, monkeys showed overall lower precision in SPEM compared to humans. This was most likely due to differences in experimental conditions, such as in the stabilization of the head, which was by a chin and a head rest in human subjects and unrestrained in monkeys. |
Suryadeep Dash; Tyler R Peel; Stephen G Lomber; Brian D Corneil Eneuro, 5 (2), pp. 1–16, 2018. @article{Dash2018, title = {Frontal eye field inactivation reduces saccade preparation in the superior colliculus but does not alter how preparatory activity relates to saccades of a given latency}, author = {Suryadeep Dash and Tyler R Peel and Stephen G Lomber and Brian D Corneil}, doi = {10.1523/eneuro.0024-18.2018}, year = {2018}, date = {2018-01-01}, journal = {Eneuro}, volume = {5}, number = {2}, pages = {1--16}, abstract = {A neural correlate for saccadic reaction times (SRTs) in the gap saccade task is the level of low-frequency activity in the intermediate layers of the superior colliculus (iSC) just before visual target onset: greater levels of such preparatory iSC low-frequency activity precede shorter SRTs. The frontal eye fields (FEFs) are one likely source of iSC preparatory activity, since FEF preparatory activity is also inversely related to SRT. To better understand the FEF's role in saccade preparation, and the way in which such preparation relates to SRT, in two male rhesus monkeys, we compared iSC preparatory activity across unilateral reversible cryogenic inactivation of the FEF. FEF inactivation increased contralesional SRTs, and lowered ipsilesional iSC preparatory activity. FEF inactivation also reduced rostral iSC activity during the gap period. Importantly, the distributions of SRTs generated with or without FEF inactivation overlapped, enabling us to conduct a novel population-level analyses examining iSC preparatory activity just before generation of SRT-matched saccades. When matched for SRTs, we observed no change during FEF inactivation in the relationship between iSC preparatory activity and SRT-matched saccades across a range of SRTs, even for the occasional express saccade. Thus, while our results emphasize that the FEF has an overall excitatory influence on preparatory activity in the iSC, the communication between the iSC and downstream oculomotor brainstem is unaltered for SRT-matched saccades.}, keywords = {}, pubstate = {published}, tppubtype = {article} } A neural correlate for saccadic reaction times (SRTs) in the gap saccade task is the level of low-frequency activity in the intermediate layers of the superior colliculus (iSC) just before visual target onset: greater levels of such preparatory iSC low-frequency activity precede shorter SRTs. The frontal eye fields (FEFs) are one likely source of iSC preparatory activity, since FEF preparatory activity is also inversely related to SRT. To better understand the FEF's role in saccade preparation, and the way in which such preparation relates to SRT, in two male rhesus monkeys, we compared iSC preparatory activity across unilateral reversible cryogenic inactivation of the FEF. FEF inactivation increased contralesional SRTs, and lowered ipsilesional iSC preparatory activity. FEF inactivation also reduced rostral iSC activity during the gap period. Importantly, the distributions of SRTs generated with or without FEF inactivation overlapped, enabling us to conduct a novel population-level analyses examining iSC preparatory activity just before generation of SRT-matched saccades. When matched for SRTs, we observed no change during FEF inactivation in the relationship between iSC preparatory activity and SRT-matched saccades across a range of SRTs, even for the occasional express saccade. Thus, while our results emphasize that the FEF has an overall excitatory influence on preparatory activity in the iSC, the communication between the iSC and downstream oculomotor brainstem is unaltered for SRT-matched saccades. |
Mohammad-Reza A Dehaqani; Abdol-Hossein Vahabie; Mohammadbagher Parsa; Behrad Noudoost; Alireza Soltani Selective changes in noise correlations contribute to an enhanced representation of saccadic targets in prefrontal neuronal ensembles Journal Article Cerebral Cortex, 28 (8), pp. 3046–3063, 2018. @article{Dehaqani2018, title = {Selective changes in noise correlations contribute to an enhanced representation of saccadic targets in prefrontal neuronal ensembles}, author = {Mohammad-Reza A Dehaqani and Abdol-Hossein Vahabie and Mohammadbagher Parsa and Behrad Noudoost and Alireza Soltani}, doi = {10.1093/cercor/bhy141}, year = {2018}, date = {2018-01-01}, journal = {Cerebral Cortex}, volume = {28}, number = {8}, pages = {3046--3063}, abstract = {An ensemble of neurons can provide a dynamic representation of external stimuli, ongoing processes, or upcoming actions. This dynamic representation could be achieved by changes in the activity of individual neurons and/or their interactions. To investigate these possibilities, we simultaneously recorded from ensembles of prefrontal neurons in non-human primates during a memory-guided saccade task. Using both decoding and encoding methods, we examined changes in the information content of individual neurons and that of ensembles between visual encoding and saccadic target selection. We found that individual neurons maintained their limited spatial sensitivity between these cognitive states, whereas the ensemble selectively improved its encoding of spatial locations far from the neurons' preferred locations. This population- level “encoding expansion” was not due to the ceiling effect at the preferred locations and was accompanied by selective changes in noise correlations for non-preferred locations. Moreover, the encoding expansion was observed for ensembles of different types of neurons and could not be explained by shifts in the preferred location of individual neurons. Our results demonstrate that the representation of space by neuronal ensembles is dynamically enhanced prior to saccades, and this enhancement occurs alongside changes in noise correlations more than changes in the activity of individual neurons.}, keywords = {}, pubstate = {published}, tppubtype = {article} } An ensemble of neurons can provide a dynamic representation of external stimuli, ongoing processes, or upcoming actions. This dynamic representation could be achieved by changes in the activity of individual neurons and/or their interactions. To investigate these possibilities, we simultaneously recorded from ensembles of prefrontal neurons in non-human primates during a memory-guided saccade task. Using both decoding and encoding methods, we examined changes in the information content of individual neurons and that of ensembles between visual encoding and saccadic target selection. We found that individual neurons maintained their limited spatial sensitivity between these cognitive states, whereas the ensemble selectively improved its encoding of spatial locations far from the neurons' preferred locations. This population- level “encoding expansion” was not due to the ceiling effect at the preferred locations and was accompanied by selective changes in noise correlations for non-preferred locations. Moreover, the encoding expansion was observed for ensembles of different types of neurons and could not be explained by shifts in the preferred location of individual neurons. Our results demonstrate that the representation of space by neuronal ensembles is dynamically enhanced prior to saccades, and this enhancement occurs alongside changes in noise correlations more than changes in the activity of individual neurons. |
Becket R Ebitz; Eddy Albarran; Tirin Moore Exploration disrupts choice-predictive signals and alters dynamics in prefrontal cortex Journal Article Neuron, 97 (2), pp. 450–461, 2018. @article{Ebitz2018, title = {Exploration disrupts choice-predictive signals and alters dynamics in prefrontal cortex}, author = {Becket R Ebitz and Eddy Albarran and Tirin Moore}, doi = {10.1016/j.neuron.2017.12.007}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {97}, number = {2}, pages = {450--461}, publisher = {Elsevier Inc.}, abstract = {In uncertain environments, decision-makers must balance two goals: they must “exploit” rewarding options but also “explore” in order to discover rewarding alternatives. Exploring and exploiting necessarily change how the brain responds to identical stimuli, but little is known about how these states, and transitions between them, change how the brain transforms sensory information into action. To address this question, we recorded neural activity in a prefrontal sensorimotor area while monkeys naturally switched between exploring and exploiting rewarding options. We found that exploration profoundly reduced spatially selective, choice-predictive activity in single neurons and delayed choice-predictive population dynamics. At the same time, reward learning was increased in brain and behavior. These results indicate that exploration is related to sudden disruptions in prefrontal sensorimotor control and rapid, reward-dependent reorganization of control dynamics. This may facilitate discovery through trial and error. Exploratory choices permit the discovery of new rewarding options. Ebitz et al. report that spatially selective, choice-predictive neurons in the prefrontal cortex do not predict choice before exploratory decisions. Reduced prefrontal control may underlie flexible decision-making and trial-and-error discovery.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In uncertain environments, decision-makers must balance two goals: they must “exploit” rewarding options but also “explore” in order to discover rewarding alternatives. Exploring and exploiting necessarily change how the brain responds to identical stimuli, but little is known about how these states, and transitions between them, change how the brain transforms sensory information into action. To address this question, we recorded neural activity in a prefrontal sensorimotor area while monkeys naturally switched between exploring and exploiting rewarding options. We found that exploration profoundly reduced spatially selective, choice-predictive activity in single neurons and delayed choice-predictive population dynamics. At the same time, reward learning was increased in brain and behavior. These results indicate that exploration is related to sudden disruptions in prefrontal sensorimotor control and rapid, reward-dependent reorganization of control dynamics. This may facilitate discovery through trial and error. Exploratory choices permit the discovery of new rewarding options. Ebitz et al. report that spatially selective, choice-predictive neurons in the prefrontal cortex do not predict choice before exploratory decisions. Reduced prefrontal control may underlie flexible decision-making and trial-and-error discovery. |
Shiva Farashahi; Habiba Azab; Benjamin Hayden; Alireza Soltani On the flexibility of basic risk attitudes in monkeys Journal Article The Journal of Neuroscience, 38 (18), pp. 4383–4398, 2018. @article{Farashahi2018, title = {On the flexibility of basic risk attitudes in monkeys}, author = {Shiva Farashahi and Habiba Azab and Benjamin Hayden and Alireza Soltani}, doi = {10.1523/jneurosci.2260-17.2018}, year = {2018}, date = {2018-01-01}, journal = {The Journal of Neuroscience}, volume = {38}, number = {18}, pages = {4383--4398}, abstract = {Monkeys and other animals appear to share with humans two risk attitudes predicted by prospect theory: an inverse-S-shaped probability weighting function and a steeper utility curve for losses than for gains. These findings suggest that such preferences are stable traits with common neural substrates. We hypothesized instead that animals tailor their preferences to subtle changes in task contexts, making risk attitudes flexible. Previous studies used a limited number of outcomes, trial types, and contexts. To gain a broader perspective, we examined two large datasets of male macaques' risky choices: one from a task with real (juice) gains and another from a token task with gains and losses. In contrast to previous findings, monkeys were risk-seeking for both gains and losses (i.e. lacked a reflection effect) and showed steeper gain than loss curves (loss-seeking). Utility curves for gains were substantially different in the two tasks. Monkeys showed nearly linear probability weightings in one task and S-shaped ones in the other; neither task produced a consistent inverse-S-shaped curve. To account for these observations, we developed and tested various computational models of the processes involved in the construction of reward value. We found that adaptive differential weighting of prospective gamble outcomes could partially account for the observed differences in the utility functions across the two experiments and thus, provide a plausible mechanism underlying flexible risk attitudes. Together, our results support the idea that risky choices are constructed flexibly at the time of elicitation and place important constraints on neural models of economic choice.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Monkeys and other animals appear to share with humans two risk attitudes predicted by prospect theory: an inverse-S-shaped probability weighting function and a steeper utility curve for losses than for gains. These findings suggest that such preferences are stable traits with common neural substrates. We hypothesized instead that animals tailor their preferences to subtle changes in task contexts, making risk attitudes flexible. Previous studies used a limited number of outcomes, trial types, and contexts. To gain a broader perspective, we examined two large datasets of male macaques' risky choices: one from a task with real (juice) gains and another from a token task with gains and losses. In contrast to previous findings, monkeys were risk-seeking for both gains and losses (i.e. lacked a reflection effect) and showed steeper gain than loss curves (loss-seeking). Utility curves for gains were substantially different in the two tasks. Monkeys showed nearly linear probability weightings in one task and S-shaped ones in the other; neither task produced a consistent inverse-S-shaped curve. To account for these observations, we developed and tested various computational models of the processes involved in the construction of reward value. We found that adaptive differential weighting of prospective gamble outcomes could partially account for the observed differences in the utility functions across the two experiments and thus, provide a plausible mechanism underlying flexible risk attitudes. Together, our results support the idea that risky choices are constructed flexibly at the time of elicitation and place important constraints on neural models of economic choice. |
Jose A Fernandez-Leon; Bryan J Hansen; Valentin Dragoi Representation of rapid image sequences in V4 Networks Journal Article Cerebral Cortex, 28 (8), pp. 2675–2684, 2018. @article{Fernandez-Leon2018, title = {Representation of rapid image sequences in V4 Networks}, author = {Jose A Fernandez-Leon and Bryan J Hansen and Valentin Dragoi}, doi = {10.1093/cercor/bhx146}, year = {2018}, date = {2018-01-01}, journal = {Cerebral Cortex}, volume = {28}, number = {8}, pages = {2675--2684}, abstract = {Natural viewing often consists of sequences of brief fixations to image patches of different structure. Whether and how briefly presented sequential stimuli are encoded in a temporal-position manner is poorly understood. Here, we performed multiple-electrode recordings in the visual cortex (area V4) of nonhuman primates (Macaca mulatta) viewing a sequence of 7 briefly flashed natural images, and measured correlations between the cue-triggered population response in the presence and absence of the stimulus. Surprisingly, we found significant correlations for images occurring at the beginning and the end of a sequence, but not for those in the middle. The correlation strength increased with stimulus exposure and favored the image position in the sequence rather than image identity. These results challenge the commonly held view that images are represented in visual cortex exclusively based on their informational content, and indicate that, in the absence of sensory information, neuronal populations exhibit reactivation of stimulus-evoked responses in a way that reflects temporal position within a stimulus sequence.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Natural viewing often consists of sequences of brief fixations to image patches of different structure. Whether and how briefly presented sequential stimuli are encoded in a temporal-position manner is poorly understood. Here, we performed multiple-electrode recordings in the visual cortex (area V4) of nonhuman primates (Macaca mulatta) viewing a sequence of 7 briefly flashed natural images, and measured correlations between the cue-triggered population response in the presence and absence of the stimulus. Surprisingly, we found significant correlations for images occurring at the beginning and the end of a sequence, but not for those in the middle. The correlation strength increased with stimulus exposure and favored the image position in the sequence rather than image identity. These results challenge the commonly held view that images are represented in visual cortex exclusively based on their informational content, and indicate that, in the absence of sensory information, neuronal populations exhibit reactivation of stimulus-evoked responses in a way that reflects temporal position within a stimulus sequence. |
Ian C Fiebelkorn; Mark A Pinsk; Sabine Kastner A dynamic interplay within the frontoparietal network underlies rhythmic spatial attention Journal Article Neuron, 99 (4), pp. 842–853, 2018. @article{Fiebelkorn2018, title = {A dynamic interplay within the frontoparietal network underlies rhythmic spatial attention}, author = {Ian C Fiebelkorn and Mark A Pinsk and Sabine Kastner}, doi = {10.1016/j.neuron.2018.07.038}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {99}, number = {4}, pages = {842--853}, publisher = {Elsevier Inc.}, abstract = {Classic studies of spatial attention assumed that its neural and behavioral effects were continuous over time. Recent behavioral studies have instead re- vealed that spatial attention leads to alternating pe- riods of heightened or diminished perceptual sensi- tivity. Yet, the neural basis of these rhythmic fluctuations has remained largely unknown. We show that a dynamic interplay within the macaque frontoparietal network accounts for the rhythmic properties of spatial attention. Neural oscillations characterize functional interactions between the frontal eye fields (FEF) and the lateral intraparietal area (LIP), with theta phase (3–8 Hz) coordinating two rhythmically alternating states. The first is defined by FEF-dominated beta-band activity, asso- ciated with suppressed attentional shifts, and LIP- dominated gamma-band activity, associated with enhanced visual processing and better behavioral performance. The second is defined by LIP-specific alpha-band activity, associated with attenuated vi- sual processing and worse behavioral performance. Our findings reveal how network-level interactions organize environmental sampling into rhythmic cycles.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Classic studies of spatial attention assumed that its neural and behavioral effects were continuous over time. Recent behavioral studies have instead re- vealed that spatial attention leads to alternating pe- riods of heightened or diminished perceptual sensi- tivity. Yet, the neural basis of these rhythmic fluctuations has remained largely unknown. We show that a dynamic interplay within the macaque frontoparietal network accounts for the rhythmic properties of spatial attention. Neural oscillations characterize functional interactions between the frontal eye fields (FEF) and the lateral intraparietal area (LIP), with theta phase (3–8 Hz) coordinating two rhythmically alternating states. The first is defined by FEF-dominated beta-band activity, asso- ciated with suppressed attentional shifts, and LIP- dominated gamma-band activity, associated with enhanced visual processing and better behavioral performance. The second is defined by LIP-specific alpha-band activity, associated with attenuated vi- sual processing and worse behavioral performance. Our findings reveal how network-level interactions organize environmental sampling into rhythmic cycles. |
Whitney S Griggs; Hidetoshi Amita; Atul Gopal; Okihide Hikosaka Visual neurons in the superior colliculus discriminate many objects by their historical values Journal Article Frontiers in Neuroscience, 12 , pp. 1–15, 2018. @article{Griggs2018, title = {Visual neurons in the superior colliculus discriminate many objects by their historical values}, author = {Whitney S Griggs and Hidetoshi Amita and Atul Gopal and Okihide Hikosaka}, doi = {10.3389/fnins.2018.00396}, year = {2018}, date = {2018-01-01}, journal = {Frontiers in Neuroscience}, volume = {12}, pages = {1--15}, abstract = {The superior colliculus (SC) is an important structure in the mammalian brain that orients the animal towards distinct visual events. Visually-responsive neurons in SC are modulated by visual object features, including size, motion, and color. However, it remains unclear whether SC activity is modulated by non-visual object features, such as the reward value associated with the object. To address this question, three monkeys were trained (textgreater10 days) to saccade to multiple fractal objects, half of which were consistently associated with large reward while other half were associated with small reward. This created historically high-valued (‘good') and low-valued (‘bad') objects. During the neuronal recordings from the SC, the monkeys maintained fixation at the center while the objects were flashed in the receptive field of the neuron without any reward. We found that approximately half of the visual neurons responded more strongly to the good than bad objects. In some neurons, this value-coding remained intact for a long time (textgreater1 year) after the last object-reward association learning. Notably, the neuronal discrimination of reward values started about 100 ms after the appearance of visual objects and lasted for more than 100 ms. These results provide evidence that SC neurons can discriminate objects by their historical (long-term) values. This object value information may be provided by the basal ganglia, especially the circuit originating from the tail of the caudate nucleus. The information may be used by the neural circuits inside SC for motor (saccade) output or may be sent to the circuits outside SC for future behavior.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The superior colliculus (SC) is an important structure in the mammalian brain that orients the animal towards distinct visual events. Visually-responsive neurons in SC are modulated by visual object features, including size, motion, and color. However, it remains unclear whether SC activity is modulated by non-visual object features, such as the reward value associated with the object. To address this question, three monkeys were trained (textgreater10 days) to saccade to multiple fractal objects, half of which were consistently associated with large reward while other half were associated with small reward. This created historically high-valued (‘good') and low-valued (‘bad') objects. During the neuronal recordings from the SC, the monkeys maintained fixation at the center while the objects were flashed in the receptive field of the neuron without any reward. We found that approximately half of the visual neurons responded more strongly to the good than bad objects. In some neurons, this value-coding remained intact for a long time (textgreater1 year) after the last object-reward association learning. Notably, the neuronal discrimination of reward values started about 100 ms after the appearance of visual objects and lasted for more than 100 ms. These results provide evidence that SC neurons can discriminate objects by their historical (long-term) values. This object value information may be provided by the basal ganglia, especially the circuit originating from the tail of the caudate nucleus. The information may be used by the neural circuits inside SC for motor (saccade) output or may be sent to the circuits outside SC for future behavior. |
Marcel Jan de Haan; Thomas Brochier; Sonja Grün; Alexa Riehle; Frédéric V Barthélemy Real-time visuomotor behavior and electrophysiology recording setup for use with humans and monkeys Journal Article Journal of Neurophysiology, 120 (2), pp. 539–552, 2018. @article{Haan2018a, title = {Real-time visuomotor behavior and electrophysiology recording setup for use with humans and monkeys}, author = {Marcel Jan de Haan and Thomas Brochier and Sonja Grün and Alexa Riehle and Frédéric V Barthélemy}, doi = {10.1152/jn.00262.2017}, year = {2018}, date = {2018-01-01}, journal = {Journal of Neurophysiology}, volume = {120}, number = {2}, pages = {539--552}, abstract = {Large-scale network dynamics in multiple visuomotor areas is of great interest in the study of eye-hand coordination in both human and monkey. To explore this, it is essential to develop a setup that allows for precise tracking of eye and hand movements. It is desirable that it is able to generate mechanical or visual perturbations of hand trajec- tories so that eye-hand coordination can be studied in a variety of conditions. There are simple solutions that satisfy these requirements for hand movements performed in the horizontal plane while visual stimuli and hand feedback are presented in the vertical plane. How- ever, this spatial dissociation requires cognitive rules for eye-hand coordination different from eye-hand movements performed in the same space, as is the case in most natural conditions. Here we present an innovative solution for the precise tracking of eye and hand movements in a single reference frame. Importantly, our solution allows behavioral explorations under normal and perturbed conditions in both humans and monkeys. It is based on the integration of two noninvasive commercially available systems to achieve online control and synchronous recording of eye (EyeLink) and hand (KINARM) positions during interactive visuomotor tasks. We also present an eye calibration method compatible with different eye trackers that com- pensates for nonlinearities caused by the system's geometry. Our setup monitors the two effectors in real time with high spatial and temporal resolution and simultaneously outputs behavioral and neu- ronal data to an external data acquisition system using a common data format.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Large-scale network dynamics in multiple visuomotor areas is of great interest in the study of eye-hand coordination in both human and monkey. To explore this, it is essential to develop a setup that allows for precise tracking of eye and hand movements. It is desirable that it is able to generate mechanical or visual perturbations of hand trajec- tories so that eye-hand coordination can be studied in a variety of conditions. There are simple solutions that satisfy these requirements for hand movements performed in the horizontal plane while visual stimuli and hand feedback are presented in the vertical plane. How- ever, this spatial dissociation requires cognitive rules for eye-hand coordination different from eye-hand movements performed in the same space, as is the case in most natural conditions. Here we present an innovative solution for the precise tracking of eye and hand movements in a single reference frame. Importantly, our solution allows behavioral explorations under normal and perturbed conditions in both humans and monkeys. It is based on the integration of two noninvasive commercially available systems to achieve online control and synchronous recording of eye (EyeLink) and hand (KINARM) positions during interactive visuomotor tasks. We also present an eye calibration method compatible with different eye trackers that com- pensates for nonlinearities caused by the system's geometry. Our setup monitors the two effectors in real time with high spatial and temporal resolution and simultaneously outputs behavioral and neu- ronal data to an external data acquisition system using a common data format. |
Christopher K Hauser; Dantong Zhu; Terrence R Stanford; Emilio Salinas Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets Journal Article eLife, 7 , pp. 1–32, 2018. @article{Hauser2018, title = {Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets}, author = {Christopher K Hauser and Dantong Zhu and Terrence R Stanford and Emilio Salinas}, doi = {10.7554/elife.33456}, year = {2018}, date = {2018-01-01}, journal = {eLife}, volume = {7}, pages = {1--32}, abstract = {In studies of voluntary movement, a most elemental quantity is the reaction time (RT) between the onset of a visual stimulus and a saccade toward it. However, this RT demonstrates extremely high variability which, in spite of extensive research, remains unexplained. It is well established that, when a visual target appears, oculomotor activity gradually builds up until a critical level is reached, at which point a saccade is triggered. Here, based on computational work and single-neuron recordings from monkey frontal eye field (FEF), we show that this rise-to-threshold process starts from a dynamic initial state that already contains other incipient, internally driven motor plans, which compete with the target-driven activity to varying degrees. The ensuing conflict resolution process, which manifests in subtle covariations between baseline activity, build-up rate, and threshold, consists of fundamentally deterministic interactions, and explains the observed RT distributions while invoking only a small amount of intrinsic randomness.As we examine the space around us our eyes move in short steps, looking toward a new location about four times a second. Neurons in a region of the brain called the frontal eye field help initiate these eye movements, which are known as saccades. Each neuron contributes to a saccade with a specific direction and size. Before a saccade, the relevant neurons in the frontal eye field steadily increase their activity. When this activity reaches a critical threshold, the visual system issues a command to move the eyes in the appropriate direction. So a saccade that moves the eyes to the right requires a specific group of neurons to be strongly activated – but, at the same time, the neurons responsible for movement to the left need to be less active.Imagine that you have to move your eyes as quickly as possible to look at a spot of light that appears on a screen. Some of the time your eyes will start to move about 100 milliseconds after the light appears. But on other attempts, your eyes will not start moving until 300 milliseconds after the light came on. What causes this variability?To find out, Hauser et al. recorded from neurons in monkeys trained to perform such a task. When the spot of light appeared many different neurons were active, suggesting there is conflict between the plan that would move the eyes toward the target and plans to look at other locations. That is, when the target appears, the monkey is already thinking of looking somewhere. The time required to resolve this conflict depends on how far apart the target and the competing locations are from one another, and on how much the competing neurons have increased their activity before the target appears.Similar mechanisms are likely to operate when we sit at the dinner table and look for the salt shaker, for example, and so the results presented by Hauser et al. will help us to understand how we direct our attention to different points in space. Understanding how these processes work in more detail will help us to discern what happens when they go wrong, as occurs in attention deficit disorders like ADHD.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In studies of voluntary movement, a most elemental quantity is the reaction time (RT) between the onset of a visual stimulus and a saccade toward it. However, this RT demonstrates extremely high variability which, in spite of extensive research, remains unexplained. It is well established that, when a visual target appears, oculomotor activity gradually builds up until a critical level is reached, at which point a saccade is triggered. Here, based on computational work and single-neuron recordings from monkey frontal eye field (FEF), we show that this rise-to-threshold process starts from a dynamic initial state that already contains other incipient, internally driven motor plans, which compete with the target-driven activity to varying degrees. The ensuing conflict resolution process, which manifests in subtle covariations between baseline activity, build-up rate, and threshold, consists of fundamentally deterministic interactions, and explains the observed RT distributions while invoking only a small amount of intrinsic randomness.As we examine the space around us our eyes move in short steps, looking toward a new location about four times a second. Neurons in a region of the brain called the frontal eye field help initiate these eye movements, which are known as saccades. Each neuron contributes to a saccade with a specific direction and size. Before a saccade, the relevant neurons in the frontal eye field steadily increase their activity. When this activity reaches a critical threshold, the visual system issues a command to move the eyes in the appropriate direction. So a saccade that moves the eyes to the right requires a specific group of neurons to be strongly activated – but, at the same time, the neurons responsible for movement to the left need to be less active.Imagine that you have to move your eyes as quickly as possible to look at a spot of light that appears on a screen. Some of the time your eyes will start to move about 100 milliseconds after the light appears. But on other attempts, your eyes will not start moving until 300 milliseconds after the light came on. What causes this variability?To find out, Hauser et al. recorded from neurons in monkeys trained to perform such a task. When the spot of light appeared many different neurons were active, suggesting there is conflict between the plan that would move the eyes toward the target and plans to look at other locations. That is, when the target appears, the monkey is already thinking of looking somewhere. The time required to resolve this conflict depends on how far apart the target and the competing locations are from one another, and on how much the competing neurons have increased their activity before the target appears.Similar mechanisms are likely to operate when we sit at the dinner table and look for the salt shaker, for example, and so the results presented by Hauser et al. will help us to understand how we direct our attention to different points in space. Understanding how these processes work in more detail will help us to discern what happens when they go wrong, as occurs in attention deficit disorders like ADHD. |
Masato Inoue; Shigeru Kitazawa Motor error in parietal area 5 and target error in area 7 drive distinctive adaptation in reaching Journal Article Current Biology, 28 , pp. 2250–2262, 2018. @article{Inoue2018, title = {Motor error in parietal area 5 and target error in area 7 drive distinctive adaptation in reaching}, author = {Masato Inoue and Shigeru Kitazawa}, doi = {10.1016/j.cub.2018.05.056}, year = {2018}, date = {2018-01-01}, journal = {Current Biology}, volume = {28}, pages = {2250--2262}, abstract = {Errors in reaching drive trial-by-trial adaptation to compensate for the error. Parietal association areas are implicated in error coding, but whether the parietal error signals directly drive adaptation remains unknown. We first examined the activity of neurons in areas 5 and 7 while two monkeys performed rapid target reaching to clarify whether and how the parietal error signals drive adaptation in reaching. We introduced random errors using a motor-driven prism device to augment random motor errors in reaching. Neurons in both regions encoded information on the target position prior to reaching and information on the motor error after reaching. However, post-movement microstimulation caused trial-by-trial adaptation to cancel the motor error only when it was delivered to area 5. By contrast, stimulation to area 7 caused trial-by-trial adaptation so that the reaching endpoint was adjusted toward the target position. We further hypothesized that area 7 would encode target error that is caused by a target jump during the reach, and our results support this hypothesis. Area 7 neurons encoded target error information, but area 5 neurons did not encode this information. These results suggest that area 5 provides signals for adapting to motor errors and that area 7 provides signals to adapt to target errors.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Errors in reaching drive trial-by-trial adaptation to compensate for the error. Parietal association areas are implicated in error coding, but whether the parietal error signals directly drive adaptation remains unknown. We first examined the activity of neurons in areas 5 and 7 while two monkeys performed rapid target reaching to clarify whether and how the parietal error signals drive adaptation in reaching. We introduced random errors using a motor-driven prism device to augment random motor errors in reaching. Neurons in both regions encoded information on the target position prior to reaching and information on the motor error after reaching. However, post-movement microstimulation caused trial-by-trial adaptation to cancel the motor error only when it was delivered to area 5. By contrast, stimulation to area 7 caused trial-by-trial adaptation so that the reaching endpoint was adjusted toward the target position. We further hypothesized that area 7 would encode target error that is caused by a target jump during the reach, and our results support this hypothesis. Area 7 neurons encoded target error information, but area 5 neurons did not encode this information. These results suggest that area 5 provides signals for adapting to motor errors and that area 7 provides signals to adapt to target errors. |