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2017 |
Maya Zhe Wang; Benjamin Y. Hayden Reactivation of associative structure specific outcome responses during prospective evaluation in reward-based choices Journal Article In: Nature communications, vol. 8, pp. 15821, 2017. @article{Wang2017e,Before making a reward-based choice, we must evaluate each option. Some theories propose that prospective evaluation involves a reactivation of the neural response to the outcome. Others propose that it calls upon a response pattern that is specific to each underlying associative structure. We hypothesize that these views are reconcilable: during prospective evaluation, offers reactivate neural responses to outcomes that are unique to each associative structure; when the outcome occurs, this pattern is activated, simultaneously, with a general response to the reward. We recorded single-units from macaque orbitofrontal cortex (Area 13) in a riskless choice task with interleaved described and experienced offer trials. Here we report that neural activations to offers and their outcomes overlap, as do neural activations to the outcomes on the two trial types. Neural activations to experienced and described offers are unrelated even though they predict the same outcomes. Our reactivation theory parsimoniously explains these results. |
Brian J. White; David J. Berg; Janis Y. Y. Kan; Robert A. Marino; Laurent Itti; Douglas P. Munoz Superior colliculus neurons encode a visual saliency map during free viewing of natural dynamic video Journal Article In: Nature Communications, vol. 8, pp. 14263, 2017. @article{White2017b,Models of visual attention postulate the existence of a saliency map whose function is to guide attention and gaze to the most conspicuous regions in a visual scene. Although cortical representations of saliency have been reported, there is mounting evidence for a subcortical saliency mechanism, which pre-dates the evolution of neocortex. Here, we conduct a strong test of the saliency hypothesis by comparing the output of a well-established computational saliency model with the activation of neurons in the primate superior colliculus (SC), a midbrain structure associated with attention and gaze, while monkeys watched video of natural scenes. We find that the activity of SC superficial visual-layer neurons (SCs), specifically, is well-predicted by the model. This saliency representation is unlikely to be inherited from fronto-parietal cortices, which do not project to SCs, but may be computed in SCs and relayed to other areas via tectothalamic pathways. |
Brian J. White; Janis Y. Y. Kan; Ron Levy; Laurent Itti; Douglas P. Munoz Superior colliculus encodes visual saliency before the primary visual cortex Journal Article In: Proceedings of the National Academy of Sciences, vol. 114, no. 35, pp. 9451–9456, 2017. @article{White2017c,Models of visual attention postulate the existence of a bottom-up saliency map that is formed early in the visual processing stream. Although studies have reported evidence of a saliency map in various cortical brain areas, determining the contribution of phylogenetically older pathways is crucial to understanding its origin. Here, we compared saliency coding from neurons in two early gateways into the visual system: the primary visual cortex (V1) and the evolutionarily older superior colliculus (SC). We found that, while the response latency to visual stimulus onset was earlier for V1 neurons than superior colliculus superficial visual-layer neurons (SCs), the saliency representation emerged earlier in SCs than in V1. Because the dominant input to the SCs arises from V1, these relative timings are consistent with the hypothesis that SCs neurons pool the inputs from multiple V1 neurons to form a feature-agnostic saliency map, which may then be relayed to other brain areas. |
Niklas Wilming; Tim C. Kietzmann; Megan Jutras; Cheng Xue; Stefan Treue; Elizabeth A. Buffalo; Peter König Differential contribution of low- and high-level image content to eye movements in monkeys and humans Journal Article In: Cerebral Cortex, vol. 27, no. 1, pp. 279–293, 2017. @article{Wilming2017,Oculomotor selection exerts a fundamental impact on our experience of the environment. To better understand the underlying principles, researchers typically rely on behavioral data from humans, and electrophysiological recordings in macaque monkeys. This approach rests on the assumption that the same selection processes are at play in both species. To test this assumption, we compared the viewing behavior of 106 humans and 11 macaques in an unconstrained free-viewing task. Our data-driven clustering analyses revealed distinct human and macaque clusters, indicating species-specific selection strategies. Yet, cross-species predictions were found to be above chance, indicating some level of shared behavior. Analyses relying on computational models of visual saliency indicate that such cross-species commonalities in free viewing are largely due to similar low-level selection mechanisms, with only a small contribution by shared higher level selection mechanisms and with consistent viewing behavior of monkeys being a subset of the consistent viewing behavior of humans. |
Kitty Z. Xu; Brian A. Anderson; Erik E. Emeric; Anthony W. Sali; Veit Stuphorn; Steven Yantis; Susan M. Courtney Neural basis of cognitive control over movement inhibition: Human fMRI and primate electrophysiology evidence Journal Article In: Neuron, vol. 96, no. 6, pp. 1447–1458.e6, 2017. @article{Xu2017,Executive control involves the ability to flexibly inhibit or change an action when it is contextually inappropriate. Using the complimentary techniques of human fMRI and monkey electrophysiology in a context-dependent stop signal task, we found a functional double dissociation between the right ventrolateral prefrontal cortex (rVLPFC) and the bi-lateral frontal eye field (FEF). Different regions of rVLPFC were associated with context-based signal meaning versus intention to inhibit a response, while FEF activity corresponded to success or failure of the response inhibition regardless of the stimulus response mapping or the context. These results were validated by electrophysiological recordings in rVLPFC and FEF from one monkey. Inhibition of a planned behavior is therefore likely not governed by a single brain system as had been previously proposed, but instead depends on two distinct neural processes involving different sub-regions of the rVLPFC and their interactions with other motor-related brain regions. Xu et al. present a rare combination of complementary evidence from human fMRI and primate neurophysiology, demonstrating that response inhibition is not directly accomplished by the rVLPFC, but instead requires multiple, distinct rVLPFC networks involving attention and contextual stimulus interpretation. |
Jacob L. Yates; Il Memming Park; Leor N. Katz; Jonathan W. Pillow; Alexander C. Huk Functional dissection of signal and noise in MT and LIP during decision-making Journal Article In: Nature Neuroscience, vol. 20, no. 9, pp. 1285–1292, 2017. @article{Yates2017,During perceptual decision-making, responses in the middle temporal (MT) and lateral intraparietal (LIP) areas appear to map onto theoretically defined quantities, with MT representing instantaneous motion evidence and LIP reflecting the accumulated evidence. However, several aspects of the transformation between the two areas have not been empirically tested. We therefore performed multistage systems identification analyses of the simultaneous activity of MT and LIP during individual decisions. We found that monkeys based their choices on evidence presented in early epochs of the motion stimulus and that substantial early weighting of motion was present in MT responses. LIP responses recapitulated MT early weighting and contained a choice-dependent buildup that was distinguishable from motion integration. Furthermore, trial-by-trial variability in LIP did not depend on MT activity. These results identify important deviations from idealizations of MT and LIP and motivate inquiry into sensorimotor computations that may intervene between MT and LIP. |
2016 |
Sujaya Neupane; Daniel Guitton; Christopher C. Pack Two distinct types of remapping in primate cortical area V4 Journal Article In: Nature Communications, vol. 7, pp. 10402, 2016. @article{Neupane2016a,Visual neurons typically receive information from a limited portion of the retina, and such receptive fields are a key organizing principle for much of visual cortex. At the same time, there is strong evidence that receptive fields transiently shift around the time of saccades. The nature of the shift is controversial: Previous studies have found shifts consistent with a role for perceptual constancy; other studies suggest a role in the allocation of spatial attention. Here we present evidence that both the previously documented functions exist in individual neurons in primate cortical area V4. Remapping associated with perceptual constancy occurs for saccades in all directions, while attentional shifts mainly occur for neurons with receptive fields in the same hemifield as the saccade end point. The latter are relatively sluggish and can be observed even during saccade planning. Overall these results suggest a complex interplay of visual and extraretinal influences during the execution of saccades. |
Nayoung So; Veit Stuphorn Supplementary eye field encodes confidence in decisions under risk Journal Article In: Cerebral Cortex, vol. 26, no. 2, pp. 764–782, 2016. @article{ss15d,Choices are made with varying degrees of confidence, a cognitive signal representing the subjective belief in the optimality of the choice. Confidence has been mostly studied in the context of perceptual judgments, in which choice accuracy can be measured using objective criteria. Here, we study confidence in subjective value-based decisions. We recorded in the supplementary eye field (SEF) of monkeys performing a gambling task, where they had to use subjective criteria for placing bets. We found neural signals in the SEF that explicitly represent choice confidence independent from reward expectation. This confidence signal appeared after the choice and diminished before the choice outcome. Most of this neuronal activity was negatively correlated with confidence, and was strongest in trials on which the monkey spontaneously withdrew his choice. Such confidence-related activity indicates that the SEF not only guides saccade selection, but also evaluates the likelihood that the choice was optimal. This internal evaluation influences decisions concerning the willingness to bear later costs that follow from the choice or to avoid them. More generally, our findings indicate that choice confidence is an integral component of all forms of decision-making, whether they are based on perceptual evidence or on value estimations. |
Leah Acker; Erica N. Pino; Edward S. Boyden; Robert Desimone FEF inactivation with improved optogenetic methods Journal Article In: Proceedings of the National Academy of Sciences, vol. 113, no. 46, pp. E7297–E7306, 2016. @article{Acker2016,Optogenetic methods have been highly effective for suppressing neural activity and modulating behavior in rodents, but effects have been much smaller in primates, which have much larger brains. Here, we present a suite of technologies to use optogenetics effectively in primates and apply these tools to a classic question in oculomotor control. First, we measured light absorption and heat propagation in vivo, optimized the conditions for using the red-light-shifted halorhodopsin Jaws in primates, and developed a large-volume illuminator to maximize light delivery with minimal heating and tissue displacement. Together, these advances allowed for nearly universal neuronal inactivation across more than 10 mm(3) of the cortex. Using these tools, we demonstrated large behavioral changes (i.e., up to several fold increases in error rate) with relatively low light power densities (≤100 mW/mm(2)) in the frontal eye field (FEF). Pharmacological inactivation studies have shown that the FEF is critical for executing saccades to remembered locations. FEF neurons increase their firing rate during the three epochs of the memory-guided saccade task: visual stimulus presentation, the delay interval, and motor preparation. It is unclear from earlier work, however, whether FEF activity during each epoch is necessary for memory-guided saccade execution. By harnessing the temporal specificity of optogenetics, we found that FEF contributes to memory-guided eye movements during every epoch of the memory-guided saccade task (the visual, delay, and motor periods). |
Hamed Zivari Adab; Rufin Vogels Perturbation of posterior inferior temporal cortical activity impairs coarse orientation discrimination Journal Article In: Cerebral Cortex, vol. 26, no. 9, pp. 3814–3827, 2016. @article{Adab2016,It is reasonable to assume that the discrimination of simple visual stimuli depends on the activity of early visual cortical neurons, because simple visual features are supposedly coded in these areas whereas more complex features are coded in late visual areas. Recently, we showed that training monkeys in a coarse orientation discrimination task modified the response properties of single neurons in the posterior inferior temporal (PIT) cortex, a late visual area. Here, we examined the contribution of PIT to coarse orientation discrimination using causal perturbation methods. Electrical stimulation (ES) of PIT with currents of at least 100 µA impaired coarse orientation discrimination in monkeys. The performance deterioration did not exclusively reflect a general impairment to perform a difficult perceptual task. However, high current (650 µA) but not low-current (100 µA) ES also impaired fine color discrimination. ES of temporal regions dorsal or anterior to PIT produced less impairment of coarse orientation discrimination than ES of PIT. Injections of the GABA agonist muscimol into PIT also impaired performance. These data suggest that the late cortical area PIT is part of the network that supports coarse orientation discrimination of a simple grating stimulus, at least after extensive training in this task at threshold. |
Jordi Aguila; Javier Cudeiro; Casto Rivadulla Effects of static magnetic fields on the visual cortex: Reversible visual deficits and reduction of neuronal activity Journal Article In: Cerebral Cortex, vol. 26, no. 2, pp. 628–638, 2016. @article{Aguila2016,Noninvasive brain stimulation techniques have been successfully used to modulate brain activity, have become a highly useful tool in basic and clinical research and, recently, have attracted increased attention due to their putative use as a method for neuro-enhancement. In this scenario, transcranial static magnetic stimulation (SMS) of moderate strength might represent an affordable, simple, and complementary method to other procedures, such as Transcranial Magnetic Stimulation or direct current stimulation, but its mechanisms and effects are not thoroughly understood. In this study, we show that static magnetic fields applied to visual cortex of awake primates cause reversible deficits in a visual detection task. Complementary experiments in anesthetized cats show that the visual deficits are a consequence of a strong reduction in neural activity. These results demonstrate that SMS is able to effectively modulate neuronal activity and could be considered to be a tool to be used for different purposes ranging from experimental studies to clinical applications. |
Evan G. Antzoulatos; Earl K. Miller Synchronous beta rhythms of frontoparietal networks support only behaviorally relevant representations Journal Article In: eLife, vol. 5, no. NOVEMBER2016, pp. 1–22, 2016. @article{Antzoulatos2016,Categorization has been associated with distributed networks of the primate brain, including the prefrontal (PFC) and posterior parietal cortices (PPC). Although category-selective spiking in PFC and PPC has been established, the frequency-dependent dynamic interactions of frontoparietal networks are largely unexplored. We trained monkeys to perform a delayed-match-to-spatial-category task while recording spikes and local field potentials from the PFC and PPC with multiple electrodes. We found category-selective beta- and delta-band synchrony between and within the areas. However, in addition to the categories, delta synchrony and spiking activity also reflected irrelevant stimulus dimensions. By contrast, beta synchrony only conveyed information about the task-relevant categories. Further, category-selective PFC neurons were synchronized with PPC beta oscillations, while neurons that carried irrelevant information were not. These results suggest that long-range beta-band synchrony could act as a filter that only supports neural representations of the variables relevant to the task at hand. |
Paul L. Aparicio; Elias B. Issa; James J. DiCarlo Neurophysiological organization of the middle face patch in macaque inferior temporal cortex Journal Article In: Journal of Neuroscience, vol. 36, no. 50, pp. 12729–12745, 2016. @article{Aparicio2016,While early cortical visual areas contain fine scale spatial organization of neuronal properties such as orientation preference, the spatial organization of higher-level visual areas is less well understood. The fMRI demonstration of face preferring regions in human ventral cortex (FFA, OFA) and monkey inferior temporal cortex ("face patches") raises the question of how neural selectivity for faces is organized. Here, we targeted hundreds of spatially registered neural recordings to the largest fMRI-identified face selective region in monkeys, the middle face patch (MFP) and show that the MFP contains a graded enrichment of face preferring neurons. At its center, as much as 93% of the sites we sampled responded twice as strongly to faces than to non-face objects. We estimate the maximum neurophysiological size of the MFP to be ∼6 mm in diameter, consistent with its previously reported size under fMRI. Importantly, face selectivity in the MFP varied strongly even between neighboring sites. Additionally, extremely face selective sites were ∼50x more likely to be present inside the MFP than outside. These results provide the first direct quantification of the size and neural composition of the MFP by showing that the cortical tissue localized to the fMRI defined region consists of a very high fraction of face preferring sites near its center, and a monotonic decrease in that fraction along any radial spatial axis. |
Iñigo Arandia-Romero; Seiji Tanabe; Jan Drugowitsch; Adam Kohn; Rubén Moreno-Bote Multiplicative and additive modulation of neuronal tuning with population activity affects encoded information Journal Article In: Neuron, vol. 89, no. 6, pp. 1305–1316, 2016. @article{ArandiaRomero2016,Numerous studies have shown that neuronal responses are modulated by stimulus properties and also by the state of the local network. However, little is known about how activity fluctuations of neuronal populations modulate the sensory tuning of cells and affect their encoded information. We found that fluctuations in ongoing and stimulus-evoked population activity in primate visual cortex modulate the tuning of neurons in a multiplicative and additive manner. While distributed on a continuum, neurons with stronger multiplicative effects tended to have less additive modulation and vice versa. The information encoded by multiplicatively modulated neurons increased with greater population activity, while that of additively modulated neurons decreased. These effects offset each other so that population activity had little effect on total information. Our results thus suggest that intrinsic activity fluctuations may act as a "traffic light" that determines which subset of neurons is most informative. |
Chadwick B. Boulay; Florian Pieper; Matthew L. Leavitt; Julio C. Martinez-Trujillo; Adam J. Sachs Single-trial decoding of intended eye movement goals from lateral prefrontal cortex neural ensembles Journal Article In: Journal of Neurophysiology, vol. 115, no. 1, pp. 486–499, 2016. @article{Boulay2016,Neurons in the lateral prefrontal cortex (LPFC) encode sensory and cognitive signals, as well as commands for goal-directed actions. Therefore, the LPFC might be a good signal source for a goal-selection brain-computer interface (BCI) that decodes the intended goal of a motor action previous to its execution. As a first step in the development of a goal-selection BCI, we set out to determine if we could decode simple behavioral intentions to direct gaze to eight different locations in space from single-trial LPFC neural activity. We recorded neuronal spiking activity from microelectrode arrays implanted in area 8A of the LPFC of two adult macaques while they made visually guided saccades to one of eight targets in a center-out task. Neuronal activity encoded target location immediately after target presentation, during a delay epoch, during the execution of the saccade, and every combination thereof. Many (40%) of the neurons that encoded target location during multiple epochs preferred different locations during different epochs. Despite heterogeneous and dynamic responses, the neuronal feature set that best predicted target location was the averaged firing rates from the entire trial and it was best classified using linear discriminant analysis (63.6$backslash$textendash96.9% in 12 sessions, mean 80.3%; information transfer rate: 21$backslash$textendash59, mean 32.8 bits/min). Our results demonstrate that it is possible to decode intended saccade target location from single-trial LPFC activity and suggest that the LPFC is a suitable signal source for a goal-selection cognitive BCI. |
Scott L. Brincat; Earl K. Miller Prefrontal cortex networks shift from external to internal modes during learning Journal Article In: Journal of Neuroscience, vol. 36, no. 37, pp. 9739–9754, 2016. @article{Brincat2016,As we learn about items in our environment, their neural representations become increasingly enriched with our acquired knowledge. But there is little understanding of how network dynamics and neural processing related to external information changes as it becomes laden with "internal" memories. We sampled spiking and local field potential activity simultaneously from multiple sites in the lateral prefrontal cortex (PFC) and the hippocampus (HPC)-regions critical for sensory associations-of monkeys performing an object paired-associate learning task. We found that in the PFC, evoked potentials to, and neural information about, external sensory stimulation decreased while induced beta-band (∼11-27 Hz) oscillatory power and synchrony associated with "top-down" or internal processing increased. By contrast, the HPC showed little evidence of learning-related changes in either spiking activity or network dynamics. The results suggest that during associative learning, PFC networks shift their resources from external to internal processing. |
Valeria C. Caruso; Daniel S. Pages; Marc A. Sommer; Jennifer M. Groh In: Journal of Neurophysiology, vol. 115, no. 6, pp. 3162–3173, 2016. @article{Caruso2016,Saccadic eye movements can be elic- ited by more than one type of sensory stimulus. This implies substantial transformations of signals originating in different sense organs as they reach a common motor output pathway. In this study, we compared the prevalence and magnitude of auditory- and visually evoked activity in a structure implicated in oculomotor processing, the primate frontal eye fields (FEF). We recorded from 324 single neurons while 2 monkeys performed delayed saccades to visual or auditory targets. We found that 64% of FEF neurons were active on presenta- tion of auditory targets and 87% were active during auditory-guided saccades, compared with 75 and 84% for visual targets and saccades. As saccade onset approached, the average level of population activity in the FEF became indistinguishable on visual and auditory trials. FEF activity was better correlated with the movement vector than with the target location for both modalities. In summary, the large proportion of auditory-responsive neurons in the FEF, the similarity between visual and auditory activity levels at the time of the saccade, and the strong correlation between the activity and the saccade vector suggest that auditory signals undergo tailoring to match roughly the strength of visual signals present in the FEF, facilitating accessing of a common motor output pathway. |
Mircea I. Chelaru; Valentin Dragoi Negative correlations in visual cortical networks Journal Article In: Cerebral Cortex, vol. 26, no. 1, pp. 246–256, 2016. @article{Chelaru2016,The amount of information encoded by cortical circuits depends critically on the capacity of nearby neurons to exhibit trial-to-trial (noise) correlations in their responses. Depending on their sign and relationship to signal correlations, noise correlations can either increase or decrease the population code accuracy relative to uncorrelated neuronal firing. Whereas positive noise correlations have been extensively studied using experimental and theoretical tools, the functional role of negative correlations in cortical circuits has remained elusive. We addressed this issue by performing multiple-electrode recording in the superficial layers of the primary visual cortex (V1) of alert monkey. Despite the fact that positive noise correlations decayed exponentially with the difference in the orientation preference between cells, negative correlations were uniformly distributed across the population. Using a statistical model for Fisher Information estimation, we found that a mild increase in negative correlations causes a sharp increase in network accuracy even when mean correlations were held constant. To examine the variables controlling the strength of negative correlations, we implemented a recurrent spiking network model of V1. We found that increasing local inhibition and reducing excitation causes a decrease in the firing rates of neurons while increasing the negative noise correlations, which in turn increase the population signal-to-noise ratio and network accuracy. Altogether, these results contribute to our understanding of the neuronal mechanism involved in the generation of negative correlations and their beneficial impact on cortical circuit function. |
Ming Chen; Peichao Li; Shude Zhu; Chao Han; Haoran Xu; Yang Fang; Jiaming Hu; Anna W. Roe; Haidong D. Lu An orientation map for motion boundaries in macaque V2 Journal Article In: Cerebral Cortex, vol. 26, no. 1, pp. 279–287, 2016. @article{Chen2016e,The ability to extract the shape of moving objects is fundamental to visual perception. However, where such computations are processed in the visual system is unknown. To address this question, we used intrinsic signal optical imaging in awake monkeys to examine cortical response to perceptual contours defined by motion contrast (motion boundaries, MBs). We found that MB stimuli elicit a robust orientation response in area V2. Orientation maps derived from subtraction of orthogonal MB stimuli aligned well with the orientation maps obtained with luminance gratings (LGs). In contrast, area V1 responded well to LGs, but exhibited a much weaker orientation response to MBs. We further show that V2 direction domains respond to motion contrast, which is required in the detection of MB in V2. These results suggest that V2 represents MB information, an important prerequisite for shape recognition and figure-ground segregation. |
M. Gabriela Costello; Dantong Zhu; Paul J. May; Emilio Salinas; Terrence R. Stanford Task dependence of decision- and choice-related activity in monkey oculomotor thalamus Journal Article In: Journal of Neurophysiology, vol. 115, no. 1, pp. 581–601, 2016. @article{Costello2016,Oculomotor signals circulate within putative recurrent feedback loops that include the frontal eye field (FEF) and the oculomotor thalamus (OcTh). To examine how OcTh contributes to visuomotor control, and perceptually informed saccadic choices in particular, neural correlates of perceptual judgment and motor selection in OcTh were evaluated and compared with those previously reported for FEF in the same subjects. Monkeys performed three tasks: a choice task in which perceptual decisions are urgent, a choice task in which identical decisions are made without time pressure, and a single-target, delayed saccade task. The OcTh yielded far fewer task-responsive neurons than the FEF, but across responsive pools, similar neuron types were found, ranging from purely visual to purely saccade related. Across such types, the impact of the perceptual information relevant to saccadic choices was qualitatively the same in FEF and OcTh. However, distinct from that in FEF, activity in OcTh was strongly task dependent, typically being most vigorous in the urgent task, less so in the easier choice task, and least in the single-target task. This was true for responsive and nonresponsive cells alike. Neurons with exclusively motor-related activity showed strong task dependence, fired less, and differed most patently from their FEF counterparts, whereas those that combined visual and motor activity fired most similarly to their FEF counterparts. The results suggest that OcTh activity is more distantly related to saccade production per se, because its degree of commitment to a motor choice varies markedly as a function of ongoing cognitive or behavioral demands. |
Yuwei Cui; Liu D. Liu; James M. McFarland; Christopher C. Pack; Daniel A. Butts Inferring cortical variability from local field potentials Journal Article In: Journal of Neuroscience, vol. 36, no. 14, pp. 4121–4135, 2016. @article{Cui2016,The responses of sensory neurons can be quite different to repeated presentations of the same stimulus. Here, we demonstrate a direct link between the trial-to-trial variability of cortical neuron responses and network activity that is reflected in local field potentials (LFPs). Spikes and LFPs were recorded with a multielectrode array from the middle temporal (MT) area of the visual cortex of macaques during the presentation of continuous optic flow stimuli. A maximum likelihood-based modeling framework was used to predict single-neuron spiking responses using the stimulus, the LFPs, and the activity of other recorded neurons. MT neuron responses were strongly linked to gamma oscillations (maximum at 40 Hz) as well as to lower-frequency delta oscillations (1-4 Hz), with consistent phase preferences across neurons. The predicted modulation associated with the LFP was largely complementary to that driven by visual stimulation, as well as the activity of other neurons, and accounted for nearly half of the trial-to-trial variability in the spiking responses. Moreover, the LFP model predictions accurately captured the temporal structure of noise correlations between pairs of simultaneously recorded neurons, and explained the variation in correlation magnitudes observed across the population. These results therefore identify signatures of network activity related to the variability of cortical neuron responses, and suggest their central role in sensory cortical function. |
Olga Dal Monte; Matthew Piva; Jason A. Morris; Steve W. C. Chang Live interaction distinctively shapes social gaze dynamics in rhesus macaques Journal Article In: Journal of Neurophysiology, vol. 116, no. 4, pp. 1626–1643, 2016. @article{DalMonte2016,The dynamic interaction of gaze between individuals is a hallmark of social cognition. However, very few studies have examined social gaze dynamics after mutual eye contact during real-time interactions. We used a highly quantifiable paradigm to assess social gaze dynamics between pairs of monkeys and modeled these dynamics using an exponential decay function to investigate sustained attention after mutual eye contact. When mon- keys were interacting with real partners compared with static images and movies of the same monkeys, we found a significant increase in the proportion of fixations to the eyes and a smaller dispersion of fixations around the eyes, indicating enhanced focal attention to the eye region. Notably, dominance and familiarity between the interact- ing pairs induced separable components of gaze dynamics that were unique to live interactions. Gaze dynamics of dominant monkeys after mutual eye contact were associated with a greater number of fixations to the eyes, whereas those of familiar pairs were associated with a faster rate of decrease in this eye-directed attention. Our findings endorse the notion that certain key aspects of social cognition are only captured during interactive social contexts and dependent on the elapsed time relative to socially meaningful events. |
Ilse C. Van Dromme; Elsie Premereur; Bram-Ernst Verhoef; Wim Vanduffel Posterior parietal cortex drives inferotemporal activations during three- dimensional object vision Journal Article In: PloS Biology, vol. 14, no. 4, pp. e1002445, 2016. @article{Dromme2016,The primate visual system consists of a ventral stream, specialized for object recognition, and a dorsal visual stream, which is crucial for spatial vision and actions. However, little is known about the interactions and information flow between these two streams. We investigated these interactions within the network processing three-dimensional (3D) object information, comprising both the dorsal and ventral stream. Reversible inactivation of the macaque caudal intraparietal area (CIP) during functional magnetic resonance imaging (fMRI) reduced fMRI activations in posterior parietal cortex in the dorsal stream and, surprisingly, also in the inferotemporal cortex (ITC) in the ventral visual stream. Moreover, CIP inactivation caused a perceptual deficit in a depth-structure categorization task. CIP-micro-stimulation during fMRI further suggests that CIP projects via posterior parietal areas to the ITC in the ventral stream. To our knowledge, these results provide the first causal evidence for the flow of visual 3D information from the dorsal stream to the ventral stream, and identify CIP as a key area for depth-structure processing. Thus, combining reversible inactivation and electrical microstimulation during fMRI provides a detailed view of the functional interactions between the two visual processing streams. |
Jacob Duijnhouwer; Bart Krekelberg Evidence and counterevidence in motion perception Journal Article In: Cerebral Cortex, vol. 26, pp. 4602–4612, 2016. @article{Duijnhouwer2016,Sensory neurons gather evidence in favor ofthe specific stimuli to which they are tuned, but they could improve their sensitivity by also taking counterevidence into account. The Bours–Lankheet model for motion detection uses counterevidence that relies on a specific combination ofthe ON and OFF channels in the early visual system. Specifically, the model detects pairs offlashes that occur separated in space and time. Ifthe flashes have the same contrast polarity, they are interpreted as evidence in favorof the corresponding motion. But if they have opposite contrasts, they are interpreted as evidence against it. This mechanism provides an explanation for reverse-phi (the perceived reversal of an apparent motion stimulus due to periodic contrast-inversions) that is a conceptual departure from the standard explanations of the effect. Here, we investigate this counterevidence mechanism by measuring directional tuning curves of neurons in the primary visual and middle temporal cortex areas of awake, behaving macaques using constant-contrast and inverting-contrast moving dot stimuli. Our electrophysiological data support the Bours–Lankheet model and suggest that the counterevidence computation occurs at an early stage of neural processing not captured by the standard models. |
Yasmine El-Shamayleh; Anitha Pasupathy Contour curvature as an invariant code for objects in visual area V4 Journal Article In: Journal of Neuroscience, vol. 36, no. 20, pp. 5532–5543, 2016. @article{ElShamayleh2016,Size-invariant object recognition-the ability to recognize objects across transformations of scale-is a fundamental feature of biological and artificial vision. To investigate its basis in the primate cerebral cortex, we measured single neuron responses to stimuli of varying size in visual area V4, a cornerstone of the object-processing pathway, in rhesus monkeys (Macaca mulatta). Leveraging two competing models for how neuronal selectivity for the bounding contours of objects may depend on stimulus size, we show that most V4 neurons (∼70%) encode objects in a size-invariant manner, consistent with selectivity for a size-independent parameter of boundary form: for these neurons, "normalized" curvature, rather than "absolute" curvature, provided a better account of responses. Our results demonstrate the suitability of contour curvature as a basis for size-invariant object representation in the visual cortex, and posit V4 as a foundation for behaviorally relevant object codes. |
David C. Godlove; Jeffrey D. Schall Microsaccade production during saccade cancelation in a stop-signal task Journal Article In: Vision Research, vol. 118, pp. 5–16, 2016. @article{Godlove2016,We obtained behavioral data to evaluate two alternative hypotheses about the neural mechanisms of gaze control. The "fixation" hypothesis states that neurons in rostral superior colliculus (SC) enforce fixation of gaze. The "microsaccade" hypothesis states that neurons in rostral SC encode microsaccades rather than fixation per se. Previously reported neuronal activity in monkey SC during the saccade stop-signal task leads to specific, dissociable behavioral predictions of these two hypotheses. When subjects are required to cancel partially-prepared saccades, imbalanced activity spreads across rostral and caudal SC with a reliable temporal profile. The microsaccade hypothesis predicts that this imbalance will lead to elevated microsaccade production biased toward the target location, while the fixation hypothesis predicts reduced microsaccade production. We tested these predictions by analyzing the microsaccades produced by 4 monkeys while they voluntarily canceled partially prepared eye movements in response to explicit stop signals. Consistent with the fixation hypothesis and contradicting the microsaccade hypothesis, we found that each subject produced significantly fewer microsaccades when normal saccades were successfully canceled. The few microsaccades escaping this inhibition tended to be directed toward the target location. We additionally investigated interactions between initiating microsaccades and inhibiting normal saccades. Reaction times were longer when microsaccades immediately preceded target presentation. However, pre-target microsaccade production did not affect stop-signal reaction time or alter the probability of canceling saccades following stop signals. These findings demonstrate that imbalanced activity within SC does not necessarily produce microsaccades and add to evidence that saccade preparation and cancelation are separate processes. |
Sarah R. Heilbronner; Benjamin Y. Hayden The description-experience gap in risky choice in nonhuman primates Journal Article In: Psychonomic Bulletin & Review, vol. 23, no. 2, pp. 593–600, 2016. @article{Heilbronner2016,Risk attitudes in humans depend on the format used to present the gamble: we are more risk-averse for common gambles in the gains domain whose properties are described to us verbally than for those whose properties we learned about solely through experience. This difference, which constitutes part ofthe description-experience gap,is important, because it highlights the role ofknowledge acquisition in decision-mak- ing. The reasons for the gap remain obscure, but could depend upon uniquely human cognitive abilities, such as those asso- ciated with language. Thus, the gap may or may not extend to nonhuman animals. For this study, rhesus monkeys performed a novel task in which the properties of some gambles were explicitly cued (described), whereas others were learned through previous choices (experienced). Our monkeys displayed a description-experience gap. Overall, monkeys were more risk-seeking for experienced than for described gambles. This difference was observed for a range ofgamble probabilities (from 20% to 80% likelihood of payoff), indicating that it is not limited to low probability events. These results suggest that the description- experience gap does not depend on uniquely human cognitive abilities, such as those associated with lan- guage, and support the idea that epistemic influences on risk attitudes are evolutionarily ancient. |
Ha Hong; Daniel L. K. Yamins; Najib J. Majaj; James J. DiCarlo Explicit information for category-orthogonal object properties increases along the ventral stream Journal Article In: Nature Neuroscience, vol. 19, no. 4, pp. 613–622, 2016. @article{Hong2016,Extensive research has revealed that the ventral visual stream hierarchically builds a robust representation for supporting visual object categorization tasks. We systematically explored the ability of multiple ventral visual areas to support a variety of 'category-orthogonal' object properties such as position, size and pose. For complex naturalistic stimuli, we found that the inferior temporal (IT) population encodes all measured category-orthogonal object properties, including those properties often considered to be low-level features (for example, position), more explicitly than earlier ventral stream areas. We also found that the IT population better predicts human performance patterns across properties. A hierarchical neural network model based on simple computational principles generates these same cross-area patterns of information. Taken together, our empirical results support the hypothesis that all behaviorally relevant object properties are extracted in concert up the ventral visual hierarchy, and our computational model explains how that hierarchy might be built. |
Guilhem Ibos; David J. Freedman Interaction between spatial and feature attention in posterior parietal cortex Journal Article In: Neuron, vol. 91, no. 4, pp. 931–943, 2016. @article{Ibos2016,Lateral intraparietal (LIP) neurons encode a vast array of sensory and cognitive variables. Recently, we proposed that the flexibility of feature representations in LIP reflect the bottom-up integration of sensory signals, modulated by feature-based attention (FBA), from upstream feature-selective cortical neurons. Moreover, LIP activity is also strongly modulated by the position of space-based attention (SBA). However, the mechanisms by which SBA and FBA interact to facilitate the representation of task-relevant spatial and non-spatial features in LIP remain unclear. We recorded from LIP neurons during performance of a task that required monkeys to detect specific conjunctions of color, motion direction, and stimulus position. Here we show that FBA and SBA potentiate each other's effect in a manner consistent with attention gating the flow of visual information along the cortical visual pathway. Our results suggest that linear bottom-up integrative mechanisms allow LIP neurons to emphasize task-relevant spatial and non-spatial features. |
Masato Inoue; Motoaki Uchimura; Shigeru Kitazawa Error signals in motor cortices drive adaptation in reaching Journal Article In: Neuron, vol. 90, no. 5, pp. 1114–1126, 2016. @article{Inoue2016,Reaching movements are subject to adaptation in response to errors induced by prisms or external perturbations. Motor cortical circuits have been hypothesized to provide execution errors that drive adaptation, but human imaging studies to date have reported that execution errors are encoded in parietal association areas. Thus, little evidence has been uncovered that supports the motor hypothesis. Here, we show that both primary motor and premotor cortices encode information on end-point errors in reaching. We further show that post-movement microstimulation to these regions caused trial-by-trial increases in errors, which subsided exponentially when the stimulation was terminated. The results indicate for the first time that motor cortical circuits provide error signals that drive trial-by-trial adaptation in reaching movements. |
Siddhartha Joshi; Yin Li; Rishi M. Kalwani; Joshua I. Gold Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex Journal Article In: Neuron, vol. 89, no. 1, pp. 221–234, 2016. @article{Joshi2016,Changes in pupil diameter that reflect effort and other cognitive factors are often interpreted in terms of the activity of norepinephrine-containing neurons in the brainstem nucleus locus coeruleus (LC), but there is little direct evidence for such a relationship. Here, we show that LC activation reliably anticipates changes in pupil diameter that either fluctuate naturally or are driven by external events during near fixation, as in many psychophysical tasks. This relationship occurs on as fine a temporal and spatial scale as single spikes from single units. However, this relationship is not specific to the LC. Similar relationships, albeit with delayed timing and different reliabilities across sites, are evident in the inferior and superior colliculus and anterior and posterior cingulate cortex. Because these regions are interconnected with the LC, the results suggest that non-luminance-mediated changes in pupil diameter might reflect LC-mediated coordination of neuronal activity throughout some parts of the brain. Joshi et al. found that changes in pupil diameter can reflect neural activity in the locus coeruleus (LC) and, less reliably, several other interconnected structures. The results suggest that LC-mediated arousal may coordinate activity throughout some parts of the brain. |
Kohitij Kar; Bart Krekelberg Testing the assumptions underlying fMRI adaptation using intracortical recordings in area MT Journal Article In: Cortex, vol. 80, pp. 21–34, 2016. @article{Kar2016,We investigated how neural activity in the middle temporal area of the macaque monkey changes after 3 sec of exposure to a visual stimulus and used this to gain insight into the assumptions underlying the fMRI adaptation method (fMRIa). We studied both changes in tuning curves following weak and strong motion stimuli (adaptation) and the differences between a first and second exposure to the same stimulus (repetition suppression). Typically, tuning curves had smaller amplitudes and narrower tuning widths after strong adaptation; this was true for single neurons, multi-unit activity (MUA), the evoked local field potential (LFP), as well as gamma band activity. Repetition typically led to reduced responses. This reduction was correlated with direction selectivity and not explained by neural fatigue. Our data, however, warn against a simplistic view of the consequences of adaptation. First, a considerable fraction of neurons and sites showed response enhancements after adaptation, especially when probed with a stimulus that moved opposite to the direction of the adapting stimulus. Second, adaptation was stimulus selective only on a time scale of ∼100 msec. Third, aggregate measures of neural activity (MUA, LFPs) had substantially different adaptation effects. Fourth, there were qualitative differences between our findings in MT and earlier findings in IT cortex. We conclude that selective adaptation effects in fMRIa are relatively easy to miss even when they exist (for instance by presenting stimuli for too long, or because neurons that enhance after adaptation cancel out the effect of neurons that suppress). Moreover, we argue that adaptation should be understood in the context of the computations that a neural circuit perform. Using fMRIa as a tool to uncover neural selectivity requires a better understanding of this circuitry and its consequences for adaptation. |
Leor N. Katz; Jacob L. Yates; Jonathan W. Pillow; Alexander C. Huk Dissociated functional significance of decision-related activity in the primate dorsal stream Journal Article In: Nature, vol. 535, pp. 285–288, 2016. @article{Katz2016,During decision making, neurons in multiple brain regions exhibit responses that are correlated with decisions. However, it remains uncertain whether or not various forms of decision-related activity are causally related to decision making. Here we address this question by recording and reversibly inactivating the lateral intraparietal (LIP) and middle temporal (MT) areas of rhesus macaques performing a motion direction discrimination task. Neurons in area LIP exhibited firing rate patterns that directly resembled the evidence accumulation process posited to govern decision making, with strong correlations between their response fluctuations and the animal's choices. Neurons in area MT, in contrast, exhibited weak correlations between their response fluctuations and choices, and had firing rate patterns consistent with their sensory role in motion encoding. The behavioural impact of pharmacological inactivation of each area was inversely related to their degree of decision-related activity: while inactivation of neurons in MT profoundly impaired psychophysical performance, inactivation in LIP had no measurable impact on decision-making performance, despite having silenced the very clusters that exhibited strong decision-related activity. Although LIP inactivation did not impair psychophysical behaviour, it did influence spatial selection and oculomotor metrics in a free-choice control task. The absence of an effect on perceptual decision making was stable over trials and sessions and was robust to changes in stimulus type and task geometry, arguing against several forms of compensation. Thus, decision-related signals in LIP do not appear to be critical for computing perceptual decisions, and may instead reflect secondary processes. Our findings highlight a dissociation between decision correlation and causation, showing that strong neuron-decision correlations do not necessarily offer direct access to the neural computations underlying decisions. |
Aarlenne Zein Khan; Douglas P. Munoz; Naomi Takahashi; Gunnar Blohm; Robert M. McPeek Effects of a pretarget distractor on saccade reaction times across space and time in monkeys and humans Journal Article In: Journal of Vision, vol. 16, no. 7, pp. 1–20, 2016. @article{Khan2016,Previous studies have shown that the influence of a behaviorally irrelevant distractor on saccade reaction times (SRTs) varies depending on the temporal and spatial relationship between the distractor and the saccade target. We measured distractor influence on SRTs to a subsequently presented target, varying the spatial location and the timing between the distractor and the target. The distractor appeared at one of four equally eccentric locations, followed by a target (either 50 ms or 200 ms after) at one of 136 different locations encompassing an area of 20° square. We extensively tested two humans and two monkeys on this task to determine interspecies similarities and differences, since monkey neurophysiology is often used to interpret human behavioral findings. Results were similar across species; for the short interval (50 ms), SRTs were shortest to a target presented close to or at the distractor location and increased primarily as a function of the distance from the distractor. There was also an effect of distractor-target direction and visual field. For the long interval (200 ms) the results were inverted; SRTs were longest for short distances between the distractor and target and decreased as a function of distance from distractor. Both SRT patterns were well captured by a two-dimensional dynamic field model with short-distance excitation and long-distance inhibition, based upon known functional connectivity found in the superior colliculus that includes wide-spread excitation and inhibition. Based on these findings, we posit that the different time-dependent patterns of distractor-related SRTs can emerge from the same underlying neuronal mechanisms common to both species. |
Rebecca M. Krock; Tirin Moore Visual sensitivity of frontal eye field neurons during the preparation of saccadic eye movements Journal Article In: Journal of Neurophysiology, vol. 116, no. 6, pp. 2882–2891, 2016. @article{Krock2016,Primate vision is continuously disrupted by saccadic eye movements, and yet this disruption goes unperceived. One mechanism thought to reduce perception of this self-generated movement is saccadic suppression, a global loss of visual sensitivity just before, during, and after saccadic eye movements. The frontal eye field (FEF) is a candidate source of neural correlates of saccadic suppression previously observed in visual cortex, because it contributes to the generation of visually guided saccades and modulates visual cortical responses. However, whether the FEF exhibits a perisaccadic reduction in visual sensitivity that could be transmitted to visual cortex is unknown. To determine whether the FEF exhibits a signature of saccadic suppression, we recorded the visual responses of FEF neurons to brief, full-field visual probe stimuli presented during fixation and before onset of saccades directed away from the receptive field in rhesus macaques (Macaca mulatta). We measured visual sensitivity during both epochs and found that it declines before saccade onset. Visual sensitivity was significantly reduced in visual but not visuomotor neurons. This reduced sensitivity was also present in visual neurons with no movement-related modulation during visually guided saccades and thus occurred independently from movement-related activity. Across the population of visual neurons, sensitivity began declining similar to 80 ms before saccade onset. We also observed a similar presaccadic reduction in sensitivity to isoluminant, chromatic stimuli. Our results demonstrate that the signaling of visual information by FEF neurons is reduced during saccade preparation, and thus these neurons exhibit a signature of saccadic suppression. |
Noah M. Ledbetter; Charles D. Chen; Ilya E. Monosov Multiple Mechanisms for Processing Reward Uncertainty in the Primate Basal Forebrain Journal Article In: Journal of Neuroscience, vol. 36, no. 30, pp. 7852–7864, 2016. @article{Ledbetter2016,The ability to use information about the uncertainty of future outcomes is critical for adaptive behavior in an uncertain world.Weshow that the basal forebrain (BF) contains at least two distinct neural-coding strategies to support this capacity. The dorsal-lateral BF, including the ventral pallidum (VP), contains reward-sensitive neurons, some of which are selectively suppressed by uncertain-reward predictions (U-). In contrast, the medial BF (mBF) contains reward-sensitive neurons, some of which are selectively enhanced (U+) by uncertain-reward predictions. In a two-alternative choice-task, U- neurons were selectively suppressed while monkeys chose uncertain options over certain options. During the same choice-epoch, U+ neurons signaled the subjective reward value of the choice options. Additionally, after the choice was reported, U+ neurons signaled reward uncertainty until the choice outcome. We suggest that uncertainty-related suppression of VP may participate in the mediation of uncertainty-seeking actions, whereas uncertainty-related enhancement of the mBF may direct cognitive resources to monitor and learn from uncertain-outcomes. |
Liu D. Liu; Ralf M. Haefner; Christopher C. Pack A neural basis for the spatial suppression of visual motion perception Journal Article In: eLife, vol. 5, pp. 1–20, 2016. @article{Liu2016c,In theory, sensory perception should be more accurate when more neurons contribute to the representation of a stimulus. However, psychophysical experiments that use larger stimuli to activate larger pools of neurons sometimes report impoverished perceptual performance. To determine the neural mechanisms underlying these paradoxical findings, we trained monkeys to discriminate the direction of motion of visual stimuli that varied in size across trials, while simultaneously recording from populations of motion-sensitive neurons in cortical area MT. We used the resulting data to constrain a computational model that explained the behavioral data as an interaction of three main mechanisms: noise correlations, which prevented stimulus information from growing with stimulus size; neural surround suppression, which decreased sensitivity for large stimuli; and a read-out strategy that emphasized neurons with receptive fields near the stimulus center. These results suggest that paradoxical percepts reflect tradeoffs between sensitivity and noise in neuronal populations. |
Lu Liu; Liang She; Ming Chen; Tianyi Liu; Haidong D. Lu; Yang Dan; Mu-ming Poo Spatial structure of neuronal receptive field in awake monkey secondary visual cortex (V2) Journal Article In: Proceedings of the National Academy of Sciences, vol. 113, no. 7, pp. 1913–1918, 2016. @article{Liu2016d,Visual processing depends critically on the receptive field (RF) properties of visual neurons. However, comprehensive characterization of RFs beyond the primary visual cortex (V1) remains a challenge. Here we report fine RF structures in secondary visual cortex (V2) of awake macaque monkeys, identified through a projection pursuit regression analysis of neuronal responses to natural images. We found that V2 RFs could be broadly classified as V1-like (typical Gabor-shaped subunits), ultralong (subunits with high aspect ratios), or complex-shaped (subunits with multiple oriented components). Furthermore, single-unit recordings from functional domains identified by intrinsic optical imaging showed that neurons with ultralong RFs were primarily localized within pale stripes, whereas neurons with complex-shaped RFs were more concentrated in thin stripes. Thus, by combining single-unit recording with optical imaging and a computational approach, we identified RF subunits underlying spatial feature selectivity of V2 neurons and demonstrated the functional organization of these RF properties. |
Mikael Lundqvist; Jonas Rose; Pawel Herman; Scott L. Brincat; Timothy J. Buschman; Earl K. Miller Gamma and beta bursts underlie working memory Journal Article In: Neuron, vol. 90, no. 1, pp. 152–164, 2016. @article{Lundqvist2016,Working memory is thought to result from sustained neuron spiking. However, computational models suggest complex dynamics with discrete oscillatory bursts. We analyzed local field potential (LFP) and spiking from the prefrontal cortex (PFC) of monkeys performing a working memory task. There were brief bursts of narrow-band gamma oscillations (45–100 Hz), varied in time and frequency, accompanying encoding and re-activation of sensory information. They appeared at a minority of recording sites associated with spiking reflecting the to-be-remembered items. Beta oscillations (20–35 Hz) also occurred in brief, variable bursts but reflected a default state interrupted by encoding and decoding. Only activity of neurons reflecting encoding/decoding correlated with changes in gamma burst rate. Thus, gamma bursts could gate access to, and prevent sensory interference with, working memory. This supports the hypothesis that working memory is manifested by discrete oscillatory dynamics and spiking, not sustained activity. |
Vincent B. McGinty; Antonio Rangel; William T. Newsome Orbitofrontal cortex value signals depend on fixation location during free viewing Journal Article In: Neuron, vol. 90, no. 6, pp. 1299–1311, 2016. @article{McGinty2016,In the natural world, monkeys and humans judge the economic value of numerous competing stimuli by moving their gaze from one object to another, in a rapid series of eye movements. This suggests that the primate brain processes value serially, and that value-coding neurons may be modulated by changes in gaze. To test this hypothesis, we presented monkeys with value-associated visual cues and took the unusual step of allowing unrestricted free viewing while we recorded neurons in the orbitofrontal cortex (OFC). By leveraging natural gaze patterns, we found that a large proportion of OFC cells encode gaze location and, that in some cells, value coding is amplified when subjects fixate near the cue. These findings provide the first cellular-level mechanism for previously documented behavioral effects of gaze on valuation and suggest a major role for gaze in neural mechanisms of valuation and decision-making under ecologically realistic conditions. |
Sujaya Neupane; Daniel Guitton; Christopher C. Pack Dissociation of forward and convergent remapping in primate visual cortex Journal Article In: Current Biology, vol. 26, no. 12, pp. R491–R492, 2016. @article{Neupane2016,A fundamental concept in neuroscience is the receptive field, the area of space over which a neuron gathers information. Until about 25 years ago, visual receptive fields were thought to be determined entirely by the pattern of retinal inputs, so it was quite surprising to find neurons in primate cortex with receptive fields that changed position every time a saccade was executed [1]. Although this discovery has figured prominently into theories of visual perception, there is still much debate about the nature of the phenomenon: Some studies report forward remapping [1–3], in which receptive fields shift to their postsaccadic locations, and others report convergent remapping, in which receptive fields shift toward the saccade target [4]. These two possibilities can be difficult to distinguish, particularly when the two types of remapping lead to receptive field shifts in similar directions [5], as was the case in virtually all previous experiments. Here we report new data from neurons in primate cortical area V4, where both types of remapping have previously been reported [3,6]. Using an experimental configuration in which forward and convergent remapping would lead to receptive field shifts in opposite directions, we show that forward remapping is the dominant type of receptive field shift in V4. |
Emily R. Oby; Sagi Perel; Patrick T. Sadtler; Douglas A. Ruff; Jessica L. Mischel; David F. Montez; Marlene R. Cohen; Aaron P. Batista; Steven M. Chase Extracellular voltage threshold settings can be tuned for optimal encoding of movement and stimulus parameters Journal Article In: Journal of Neural Engineering, vol. 13, no. 3, pp. 1–15, 2016. @article{Oby2016,OBJECTIVE: A traditional goal of neural recording with extracellular electrodes is to isolate action potential waveforms of an individual neuron. Recently, in brain-computer interfaces (BCIs), it has been recognized that threshold crossing events of the voltage waveform also convey rich information. To date, the threshold for detecting threshold crossings has been selected to preserve single-neuron isolation. However, the optimal threshold for single-neuron identification is not necessarily the optimal threshold for information extraction. Here we introduce a procedure to determine the best threshold for extracting information from extracellular recordings. We apply this procedure in two distinct contexts: the encoding of kinematic parameters from neural activity in primary motor cortex (M1), and visual stimulus parameters from neural activity in primary visual cortex (V1). APPROACH: We record extracellularly from multi-electrode arrays implanted in M1 or V1 in monkeys. Then, we systematically sweep the voltage detection threshold and quantify the information conveyed by the corresponding threshold crossings. MAIN RESULTS: The optimal threshold depends on the desired information. In M1, velocity is optimally encoded at higher thresholds than speed; in both cases the optimal thresholds are lower than are typically used in BCI applications. In V1, information about the orientation of a visual stimulus is optimally encoded at higher thresholds than is visual contrast. A conceptual model explains these results as a consequence of cortical topography. SIGNIFICANCE: How neural signals are processed impacts the information that can be extracted from them. Both the type and quality of information contained in threshold crossings depend on the threshold setting. There is more information available in these signals than is typically extracted. Adjusting the detection threshold to the parameter of interest in a BCI context should improve our ability to decode motor intent, and thus enhance BCI control. Further, by sweeping the detection threshold, one can gain insights into the topographic organization of the nearby neural tissue. |
Tyler R. Peel; Ziad M. Hafed; Suryadeep Dash; Stephen G. Lomber; Brian D. Corneil A causal role for the cortical frontal eye fields in microsaccade deployment Journal Article In: PLoS Biology, vol. 14, no. 8, pp. e1002531, 2016. @article{Peel2016,Microsaccades aid vision by helping to strategically sample visual scenes. Despite the importance of these small eye movements, no cortical area has ever been implicated in their generation. Here, we used unilateral and bilateral reversible inactivation of the frontal eye fields (FEF) to identify a cortical drive for microsaccades. Unexpectedly, FEF inactivation altered microsaccade metrics and kinematics. Such inactivation also impaired microsaccade deployment following peripheral cue onset, regardless of cue side or inactivation configuration. Our results demonstrate that the FEF provides critical top-down drive for microsaccade generation, particularly during the recovery of microsaccades after disruption by sensory transients. Our results constitute the first direct evidence, to our knowledge, for the contribution of any cortical area to microsaccade generation, and they provide a possible substrate for how cognitive processes can influence the strategic deployment of microsaccades. |
Ivo D. Popivanov; Philippe G. Schyns; Rufin Vogels Stimulus features coded by single neurons of a macaque body category selective patch Journal Article In: Proceedings of the National Academy of Sciences, vol. 113, no. 17, pp. E2450–E2459, 2016. @article{Popivanov2016,Body category-selective regions of the primate temporal cortex respond to images of bodies, but it is unclear which fragments of such images drive single neurons' responses in these regions. Here we applied the Bubbles technique to the responses of single macaque middle superior temporal sulcus (midSTS) body patch neurons to reveal the image fragments the neurons respond to. We found that local image fragments such as extremities (limbs), curved boundaries, and parts of the torso drove the large majority of neurons. Bubbles revealed the whole body in only a few neurons. Neurons coded the features in a manner that was tolerant to translation and scale changes. Most image fragments were excitatory but for a few neurons both inhibitory and excitatory fragments (opponent coding) were present in the same image. The fragments we reveal here in the body patch with Bubbles differ from those suggested in previous studies of face-selective neurons in face patches. Together, our data indicate that the majority of body patch neurons respond to local image fragments that occur frequently, but not exclusively, in bodies, with a coding that is tolerant to translation and scale. Overall, the data suggest that the body category selectivity of the midSTS body patch depends more on the feature statistics of bodies (e.g., extensions occur more frequently in bodies) than on semantics (bodies as an abstract category). |
Maria C. Romero; Peter Janssen Receptive field properties of neurons in the macaque anterior intraparietal area Journal Article In: Journal of Neurophysiology, vol. 115, no. 3, pp. 1542–1555, 2016. @article{rj16,Visual object information is necessary for grasping. In primates, the anterior intraparietal area (AIP) plays an essential role in visually guided grasping. Neurons in AIP encode features of objects, but no study has systematically investigated the receptive field (RF) of AIP neurons. We mapped the RF of posterior AIP (pAIP) neurons in the central visual field, using images of objects and small line fragments that evoked robust responses, together with less effective stimuli. The RF sizes we measured varied between 3°(2)and 90°(2), with the highest response either at the fixation point or at parafoveal positions. A large fraction of pAIP neurons showed nonuniform RFs, with multiple local maxima in both ipsilateral and contralateral hemifields. Moreover, the RF profile could depend strongly on the stimulus used to map the RF. Highly similar results were obtained with the smallest stimulus that evoked reliable responses (line fragments measuring 1-2°). The nonuniformity and dependence of the RF profile on the stimulus in pAIP were comparable to previous observations in the anterior part of the lateral intraparietal area (aLIP), but the average RF of pAIP neurons was located at the fovea whereas the average RF of aLIP neurons was located parafoveally. Thus nonuniformity and stimulus dependence of the RF may represent general RF properties of neurons in the dorsal visual stream involved in object analysis, which contrast markedly with those of neurons in the ventral visual stream. |
Douglas A. Ruff; Joshua J. Alberts; Marlene R. Cohen Relating normalization to neuronal populations across cortical areas Journal Article In: Journal of Neurophysiology, vol. 116, no. 3, pp. 1375–1386, 2016. @article{rac16,Normalization, which divisively scales neuronal responses to multiple stimuli, is thought to underlie many sensory, motor, and cognitive processes. In every study where it has been investigated, neurons measured in the same brain area under identical conditions exhibit a range of normalization, ranging from suppression by nonpreferred stimuli (strong normalization) to additive responses to combinations of stimuli (no normalization; for examples, Lee and Maunsell, 2009; Busse et al., 2009). Normalization has been hypothesized to arise from interactions between neuronal populations, either in the same or different brain areas (Heeger, 1992; Carandini et al., 1997; Carandini and Heeger, 2012; Busse et al., 2009; Chance et al., 2002; Rubin et al., 2013; Rust et al., 2006; Sit et al., 2009), but current models of normalization are not mechanistic and focus on trial-averaged responses. To gain insight into the mechanisms underlying normalization, we examined interactions between neurons that exhibit different degrees of normalization. We recorded from multiple neurons in three cortical areas while rhesus monkeys viewed superimposed drifting gratings. We found that neurons showing strong normalization shared less trial-to-trial variability with other neurons in the same cortical area and more variability with neurons in other cortical areas than did units with weak normalization. Furthermore, the cortical organization of normalization was not random: neurons recorded on nearby electrodes tended to exhibit similar amounts of normalization. Together, our results suggest that normalization reflects a neuron's role in its local network and that modulatory factors like normalization share the topographic organization typical of sensory tuning properties. |
Douglas A. Ruff; Marlene R. Cohen Stimulus dependence of correlated variability across cortical areas Journal Article In: Journal of Neuroscience, vol. 36, no. 28, pp. 7546–7556, 2016. @article{Ruff2016,The way that correlated trial-to-trial variability between pairs ofneurons in the same brain area (termed spike count or noise correlation, rSC) depends on stimulus or task conditions can constrain models ofcortical circuits and ofthe computations performed by networks of neurons (Cohen and Kohn, 2011). In visual cortex, rSC tends not to depend on stimulus properties (Kohn and Smith, 2005; Huang and Lisberger, 2009) but does depend on cognitive factors like visual attention (Cohen and Maunsell, 2009; Mitchell et al., 2009). However, neurons across visual areas respond to any visual stimulus or contribute to any perceptual decision, and the way that information from multiple areas is combined to guide perception is unknown. To gain insight into these issues, we recorded simultaneously from neurons in two areas ofvisual cortex (primary visual cortex, V1, and the middle temporal area, MT) while rhesus monkeys viewed different visual stimuli in different attention conditions.Wefound that correlations betweenneurons in different areasdependonstimulusandattention conditions in very different ways than do correlations within an area. Correlations across, but not within, areas depend on stimulus direction and the presence ofa second stimulus, and attention has opposite effects on correlations within and across areas. This observed pattern ofcross-area correlations is predicted bya normalization model whereMTunits sumV1 inputs that are passed through a divisive nonlinearity. Together, our results provide insight into how neurons in different areas interact and constrain models of the neural computations performed across cortical areas. |
Douglas A. Ruff; Marlene R. Cohen Attention increases spike count correlations between visual cortical areas Journal Article In: Journal of Neuroscience, vol. 36, no. 28, pp. 7523–7534, 2016. @article{rc16,Visual attention, which improves perception of attended locations or objects, has long been known to affect many aspects of the responses of neuronal populations in visual cortex. There are two nonmutually exclusive hypotheses concerning the neuronal mechanisms that underlie these perceptual improvements. The first hypothesis, that attention improves the information encoded by a population of neurons in a particular cortical area, has considerable physiological support. The second hypothesis is that attention improves perception by selectively communicating relevant visual information. This idea has been tested primarily by measuring interactions between neurons on very short timescales, which are mathematically nearly independent of neuronal interactions on longer timescales. We tested the hypothesis that attention changes the way visual information is communicated between cortical areas on longer timescales by recording simultaneously from neurons in primary visual cortex (V1) and the middle temporal area (MT) in rhesus monkeys. We used two independent and complementary approaches. Our correlative experiment showed that attention increases the trial-to-trial response variability that is shared between the two areas. In our causal experiment, we electrically microstimulated V1 and found that attention increased the effect of stimulation on MT responses. Together, our results suggest that attention affects both the way visual stimuli are encoded within a cortical area and the extent to which visual information is communicated between areas on behaviorally relevant timescales. |
Arup Sarma; Nicolas Y. Masse; Xiao-Jing Wang; David J. Freedman Task-specific versus generalized mnemonic representations in parietal and prefrontal cortices Journal Article In: Nature Neuroscience, vol. 19, no. 1, pp. 143–149, 2016. @article{Sarma2015,Our ability to learn a wide range of behavioral tasks is essential for responding appropriately to sensory stimuli according to behavioral demands, but the underlying neural mechanism has been rarely examined by neurophysiological recordings in the same subjects across learning. To understand how learning new behavioral tasks affects neuronal representations, we recorded from posterior parietal cortex (PPC) before and after training on a visual motion categorization task. We found that categorization training influenced cognitive encoding in PPC, with a marked enhancement of memory-related delay-period encoding during the categorization task that was absent during a motion discrimination task before categorization training. In contrast, the prefrontal cortex (PFC) exhibited strong delay-period encoding during both discrimination and categorization tasks. This reveals a dissociation between PFC's and PPC's roles in working memory, with general engagement of PFC across multiple tasks, in contrast with more task-specific mnemonic encoding in PPC. |
Eyal Seidemann; Yuzhi Chen; Yoon Bai; Spencer C. Chen; Preeti Mehta; Bridget L. Kajs; Wilson S. Geisler; Boris V. Zemelman Calcium imaging with genetically encoded indicators in behaving primates Journal Article In: eLife, vol. 5, pp. 1–19, 2016. @article{Seidemann2016,Understanding the neural basis of behaviour requires studying brain activity in behaving subjects using complementary techniques that measure neural responses at multiple spatial scales, and developing computational tools for understanding the mapping between these measurements. Here we report the first results of widefield imaging of genetically encoded calcium indicator (GCaMP6f) signals from V1 of behaving macaques. This technique provides a robust readout of visual population responses at the columnar scale over multiple mm(2) and over several months. To determine the quantitative relation between the widefield GCaMP signals and the locally pooled spiking activity, we developed a computational model that sums the responses of V1 neurons characterized by prior single unit measurements. The measured tuning properties of the GCaMP signals to stimulus contrast, orientation and spatial position closely match the predictions of the model, suggesting that widefield GCaMP signals are linearly related to the summed local spiking activity. |
Kevin J. Skoblenick; Thilo Womelsdorf; Stefan Everling Ketamine alters outcome-related local field potentials in monkey prefrontal cortex Journal Article In: Cerebral Cortex, vol. 26, no. 6, pp. 2743–2752, 2016. @article{swe15,A subanesthetic dose of the noncompetitive N-methyl-d-aspartate receptor antagonist ketamine is known to induce a schizophrenia-like phenotype in humans and nonhuman primates alike. The transient behavioral changes mimic the positive, negative, and cognitive symptoms of the disease but the neural mechanisms behind these changes are poorly understood. A growing body of evidence indicates that the cognitive control processes associated with prefrontal cortex (PFC) regions relies on groups of neurons synchronizing at narrow-band frequencies measurable in the local field potential (LFP). Here,we recorded LFPs from the caudo-lateral PFC of 2 macaque monkeys performing an antisaccade task, which requires the suppression of an automatic saccade toward a stimulus and the initiation of a goal-directed saccade in the opposite direction. Preketamine injection activity showed significant differences in a narrow 20–30 Hz beta frequency band between correct and error trials in the postsaccade response epoch. Ketamine significantly impaired the animals' performance and was associated with a loss of the differences in outcome-specific beta-band power. Instead, we observed a large increase in high-gamma-band activity. Our results suggest that the PFC employs beta-band synchronization to prepare for top–down cognitive control of saccades and the monitoring of task outcome. |
B. J. Sleezer; M. D. Castagno; Benjamin Y. Hayden Rule encoding in orbitofrontal cortex and striatum guides selection Journal Article In: Journal of Neuroscience, vol. 36, no. 44, pp. 11223–11237, 2016. @article{sch16,Active maintenance of rules, like other executive functions, is often thought to be the domain of a discrete executive system. Analternative view is that rule maintenance is a broadly distributed function relying on widespread cortical and subcortical circuits. Tentative evidence supporting this view comes from research showing some rule selectivity in the orbitofrontal cortex and dorsal striatum. We recorded in these regions and in the ventral striatum, which has not been associated previously with rule representation, as macaques performed a Wisconsin Card Sorting Task. We found robust encoding ofrule category (color vs shape) and rule identity (six possible rules) in all three regions. Rule identity modulated responses to potential choice targets, suggesting that rule information guides behavior by highlighting choice targets. The effects that we observed were not explained by differences in behavioral performance across rules and thus cannot be attributed to reward expectation. Our results suggest that rule maintenance and rule-guided selection of options are distributed processes and provide new insight into orbital and striatal contributions to executive control. |
Brianna J. Sleezer; Benjamin Y. Hayden Differential contributions of ventral and dorsal striatum to early and late phases of cognitive set reconfiguration Journal Article In: Journal of Cognitive Neuroscience, vol. 28, no. 12, pp. 1849–1864, 2016. @article{Sleezer2016,Flexible decision-making, a defining feature of human cognition, is typically thought of as a canonical pFC function. Recent work suggests that the striatum may participate as well; however, its role in this process is not well understood. We recorded activity of neurons in both the ventral (VS) and dorsal (DS) striatum while rhesus macaques performed a version of the Wisconsin Card Sorting Test, a classic test of flexibility. Our version of the task involved a trial-and-error phase before monkeys could identify the correct rule on each block. We observed changes in firing rate in both regions when monkeys switched rules. Specifically, VS neurons demonstrated switch-related activity early in the trial-and-error period when the rule needed to be updated, and a portion of these neurons signaled information about the switch context (i.e., whether the switch was intradimensional or extradimensional). Neurons in both VS and DS demonstrated switch-related activity at the end of the trial-and-error period, immediately before the rule was fully established and main- tained, but these signals did not carry any information about switch context. We also observed associative learning signals (i.e., specific responses to options associated with rewards in the presentation period before choice) that followed the same pattern as switch signals (early in VS, later in DS). Taken together, these results endorse the idea that the striatum participates directly in cognitive set reconfiguration and suggest that single neurons in the striatum may contribute to a functional handoff from the VS to the DS during reconfiguration processes. |
Adam C. Snyder; Michael J. Morais; Matthew A. Smith Dynamics of excitatory and inhibitory networks are differentially altered by selective attention Journal Article In: Journal of Neurophysiology, vol. 116, no. 4, pp. 1807–1820, 2016. @article{sms16,Inhibition and excitation form two fundamental modes of neuronal interaction, yet we understand relatively little about their distinct roles in service of perceptual and cognitive processes. We developed a multidimensional waveform analysis to identify fast-spiking (putative inhibitory) and regular-spiking (putative excitatory) neurons in vivo and used this method to analyze how attention affects these two cell classes in visual area V4 of rhesus macaques. We found that putative inhibitory neurons had both greater increases in firing rate and decreases in correlated variability with attention when compared to putative excitatory neurons. Moreover, the time course of attention effects for putative inhibitory neurons more closely tracked the temporal statistics of target probability in our task. Finally, the session-to-session variability in a behavioral measure of attention co-varied with the magnitude of this effect. Together, these results suggest that selective targeting of inhibitory neurons and networks is a critical mechanism for attentional modulation. |
Caleb E. Strait; Brianna J. Sleezer; Tommy C. Blanchard; Habiba Azab; Meghan D. Castagno; Benjamin Y. Hayden Neuronal selectivity for spatial positions of offers and choices in five reward regions Journal Article In: Journal of Neurophysiology, vol. 115, no. 3, pp. 1098–1111, 2016. @article{Strait2016,When we evaluate an option, how is the neural representation of its value linked to information that identifies it, such as its position in space? We hypothesized that value information and identity cues are not bound together at a particular point but are represented together at the single unit level throughout the entirety of the choice process. We examined neuronal responses in two-option gambling tasks with lateralized and asynchronous presentation of offers in five reward regions: orbitofrontal cortex (OFC, area 13), ventromedial prefrontal cortex (vmPFC, area 14), ventral striatum (VS), dorsal anterior cingulate cortex (dACC), and subgenual anterior cingulate cortex (sgACC, area 25). Neuronal responses in all areas are sensitive to the positions of both offers and of choices. This selectivity is strongest in reward-sensitive neurons, indicating that it is not a property of a specialized subpopulation of cells. We did not find consistent contralateral or any other organization to these responses, indicating that they may be difficult to detect with aggregate measures like neuro-imaging or studies of lesion effects. These results suggest that value coding is wed to factors that identify the object throughout the reward system and suggest a possible solution to the binding problem raised by abstract value encoding schemes. |
Jessica Taubert; Valerie Goffaux; Goedele Van Belle; Wim Vanduffel; Rufin Vogels The impact of orientation filtering on face-selective neurons in monkey inferior temporal cortex Journal Article In: Scientific Reports, vol. 6, pp. 21189, 2016. @article{Taubert2016,Faces convey complex social signals to primates. These signals are tolerant of some image transformations (e.g. changes in size) but not others (e.g. picture-plane rotation). By filtering face stimuli for orientation content, studies of human behavior and brain responses have shown that face processing is tuned to selective orientation ranges. In the present study, for the first time, we recorded the responses of face-selective neurons in monkey inferior temporal (IT) cortex to intact and scrambled faces that were filtered to selectively preserve horizontal or vertical information. Guided by functional maps, we recorded neurons in the lateral middle patch (ML), the lateral anterior patch (AL), and an additional region located outside of the functionally defined face-patches (CONTROL). We found that neurons in ML preferred horizontal-passed faces over their vertical-passed counterparts. Neurons in AL, however, had a preference for vertical-passed faces, while neurons in CONTROL had no systematic preference. Importantly, orientation filtering did not modulate the firing rate of neurons to phase-scrambled face stimuli in any recording region. Together these results suggest that face-selective neurons found in the face-selective patches are differentially tuned to orientation content, with horizontal tuning in area ML and vertical tuning in area AL. |
Bram-Ernst Verhoef; John H. R. Maunsell Attention operates uniformly throughout the classical receptive field and the surround Journal Article In: eLife, vol. 5, no. AUGUST, pp. 1–16, 2016. @article{Verhoef2016,Shifting attention among visual stimuli at different locations modulates neuronal responses in heterogeneous ways, depending on where those stimuli lie within the receptive fields of neurons. Yet how attention interacts with the receptive-field structure of cortical neurons remains unclear. We measured neuronal responses in area V4 while monkeys shifted their attention among stimuli placed in different locations within and around neuronal receptive fields. We found that attention interacts uniformly with the spatially-varying excitation and suppression associated with the receptive field. This interaction explained the large variability in attention modulation across neurons, and a non-additive relationship among stimulus selectivity, stimulus-induced suppression and attention modulation that has not been previously described. A spatially-tuned normalization model precisely accounted for all observed attention modulations and for the spatial summation properties of neurons. These results provide a unified account of spatial summation and attention-related modulation across both the classical receptive field and the surround. |
Susheel Vijayraghavan; Alex James Major; Stefan Everling Dopamine D1 and D2 Receptors Make Dissociable Contributions to Dorsolateral Prefrontal Cortical Regulation of Rule-Guided Oculomotor Behavior Journal Article In: Cell Reports, vol. 16, no. 3, pp. 805–816, 2016. @article{Vijayraghavan2016,Studies of neuromodulation of spatial short-term memory have shown that dopamine D1 receptor (D1R) stimulation in dorsolateral prefrontal cortex (DLPFC) dose-dependently modulates memory activity, whereas D2 receptors (D2Rs) selectively modulate activity related to eye movements hypothesized to encode movement feedback. We examined localized stimulation of D1Rs and D2Rs on DLPFC neurons engaged in a task involving rule representation in memory to guide appropriate eye movements toward or away from a visual stimulus. We found dissociable effects of D1R and D2R on DLPFC physiology. D1R stimulation degrades memory activity for the task rule and increases stimulus-related selectivity. In contrast, D2R stimulation affects motor activity tuning only when eye movements are made to the stimulus. Only D1R stimulation degrades task performance and increases impulsive responding. Our results suggest that D1Rs regulate rule representation and impulse control, whereas D2Rs selectively modulate eye-movement-related dynamics and not rule representation in the DLPFC. |
Nicolas Wattiez; Tymothée Poitou; Sophie Rivaud-Péchoux; Pierre Pouget Evidence for spatial tuning of movement inhibition Journal Article In: Experimental Brain Research, vol. 234, no. 7, pp. 1957–1966, 2016. @article{Wattiez2016,The time to initiate a movement can, even implicitly, be influenced by the environment. All primates, including humans, respond faster and with greater accuracy to stimuli that are brighter, louder or associated with larger reward, than to neutral stimuli. Whether this environment also modulates the executive functions which allow ongoing actions to be suppressed remains an issue of debate. In this study, we investigated the implicit learning of spatial selectivity of movement inhibition in humans and macaque monkeys performing a saccade-countermanding task. The occurrence of stop trials, in which subjects were visually instructed to cancel a prepared movement, was manipulated according to the target location. One visual target was associated with higher probability of stop signal appearance (e.g., 80 %), while the second target was associated with low fraction of stop (e.g., 20 %). The absolute occurrence of stop trials across the two targets (50 %) remains constant. The results show that human and macaque monkeys can selectively adapt their behaviors according to the implicit probability of stopping. Behavioral adjustments were larger when targets were in different hemifields and for larger distances between targets. Reduced selective inhibitory behaviors were observed when 15 degrees of visual angle separated the targets, and this effect vanished when targets were separated by only 2 degrees . Overall, our study shows that both response and inhibition times can be modulated by the relative spatial occurrence of stop signals. We speculate that beyond the particular effect we observed in the context of the saccade paradigm, selective motor execution may imply a disinhibitory mechanism that modulates the motor pathways associated with the fronto-median cortex and basal ganglia circuits. |
J. Kael White; Ilya E. Monosov Neurons in the primate dorsal striatum signal the uncertainty of object-reward associations Journal Article In: Nature Communications, vol. 7, pp. 12735, 2016. @article{White2016b,To learn, obtain reward and survive, humans and other animals must monitor, approach and act on objects that are associated with variable or unknown rewards. However, the neuronal mechanisms that mediate behaviours aimed at uncertain objects are poorly understood. Here we demonstrate that a set of neurons in an internal-capsule bordering regions of the primate dorsal striatum, within the putamen and caudate nucleus, signal the uncertainty of object– reward associations. Their uncertainty responses depend on the presence of objects asso- ciated with reward uncertainty and evolve rapidly as monkeys learn novel object–reward associations. Therefore, beyond its established role in mediating actions aimed at known or certain rewards, the dorsal striatum also participates in behaviours aimed at reward-uncertain objects. |
Jue Xie; Camillo Padoa-Schioppa Neuronal remapping and circuit persistence in economic decisions Journal Article In: Nature Neuroscience, vol. 19, no. 6, pp. 855–861, 2016. @article{Xie2016,The orbitofrontal cortex plays a central role in good-based economic decisions. When subjects make choices, neurons in this region represent the identities and values of offered and chosen goods. Notably, choices in different behavioral contexts may involve a potentially infinite variety of goods. Thus a fundamental question concerns the stability versus flexibility of the decision circuit. Here we show in rhesus monkeys that neurons encoding the identity or the subjective value of particular goods in a given context 'remap' and become associated with different goods when the context changes. At the same time, the overall organization of the decision circuit and the function of individual cells remain stable across contexts. In particular, two neurons supporting the same decision in one context also support the same decision in different contexts. These results demonstrate how the same neural circuit can underlie economic decisions involving a large variety of goods. |
Tao Yao; Stefan Treue; B. Suresh Krishna An attention-sensitive memory trace in macaque MT following saccadic eye movements Journal Article In: PLoS Biology, vol. 14, no. 2, pp. e1002390, 2016. @article{Yao2016,We experience a visually stable world despite frequent retinal image displacements induced by eye, head, and body movements. The neural mechanisms underlying this remain unclear. One mechanism that may contribute is transsaccadic remapping, in which the responses of some neurons in various attentional, oculomotor, and visual brain areas appear to anticipate the consequences of saccades. The functional role of transsaccadic remapping is actively debated, and many of its key properties remain unknown. Here, recording from two monkeys trained to make a saccade while directing attention to one of two spatial locations, we show that neurons in the middle temporal area (MT), a key locus in the motion-processing pathway of humans and macaques, show a form of transsaccadic remapping called a memory trace. The memory trace in MT neurons is enhanced by the allocation of top-down spatial attention. Our data provide the first demonstration, to our knowledge, of the influence of top-down attention on the memory trace anywhere in the brain. We find evidence only for a small and transient effect of motion direction on the memory trace (and in only one of two monkeys), arguing against a role for MT in the theoretically critical yet empirically contentious phenomenon of spatiotopic feature-comparison and adaptation transfer across saccades. Our data support the hypothesis that transsaccadic remapping represents the shift of attentional pointers in a retinotopic map, so that relevant locations can be tracked and rapidly processed across saccades. Our results resolve important issues concerning the perisaccadic representation of visual stimuli in the dorsal stream and demonstrate a significant role for top-down attention in modulating this representation. |
Gongchen Yu; Baijie Xu; Yuchen Zhao; Beizhen Zhang; Mingpo Yang; Janis Y. Y. Kan; David M. Milstein; Dhushan Thevarajah; Michael C. Dorris Microsaccade direction reflects the economic value of potential saccade goals and predicts saccade choice Journal Article In: Journal of Neurophysiology, vol. 115, no. 2, pp. 741–751, 2016. @article{Yu2016b,Microsaccades are small-amplitude (typically <1°), ballistic eye movements that occur when attempting to fixate gaze. Initially thought to be generated randomly, it has recently been established that microsaccades are influenced by sensory stimuli, attentional processes, and certain cognitive states. Whether decision processes influence microsaccades, however, is unknown. Here, we adapted two classic economic tasks to examine whether microsaccades reflect evolving saccade decisions. Volitional saccade choices of monkey and human subjects provided a measure of the subjective value of targets. Importantly, analyses occurred during a period of complete darkness to minimize the known influence of sensory and attentional processes on microsaccades. As the time of saccadic choice approached, microsaccade direction became the following: 1) biased toward targets as a function of their subjective value and 2) predictive of upcoming, voluntary choice. Our results indicate that microsaccade direction is influenced by and is a reliable tell of evolving saccade decisions. Our results are consistent with dynamic decision processes within the midbrain superior colliculus; that is, microsaccade direction is influenced by the transition of activity toward caudal saccade regions associated with high saccade value and/or future saccade choice. |
Theodoros P. Zanos; Patrick J. Mineault; Daniel Guitton; Christopher C. Pack Mechanisms of saccadic suppression in primate cortical area V4 Journal Article In: Journal of Neuroscience, vol. 36, no. 35, pp. 9227–9239, 2016. @article{Zanos2016,Psychophysical studies have shown that subjects are often unaware of visual stimuli presented around the time of an eye movement. This saccadic suppression is thought to be a mechanism for maintaining perceptual stability. The brain might accomplish saccadic suppression by reducing the gain of visual responses to specific stimuli or by simply suppressing firing uniformly for all stimuli. Moreover, the suppression might be identical across the visual field or concentrated at specific points. To evaluate these possibilities, we recorded from individual neurons in cortical area V4 of nonhuman primates trained to execute saccadic eye movements. We found that both modes of suppression were evident in the visual responses of these neurons and that the two modes showed different spatial and temporal profiles: while gain changes started earlier and were more widely distributed across visual space, nonspecific suppression was found more often in the peripheral visual field, after the completion of the saccade. Peripheral suppression was also associated with increased noise correlations and stronger local field potential oscillations in the α frequency band. This pattern of results suggests that saccadic suppression shares some of the circuitry responsible for allocating voluntary attention. SIGNIFICANCE STATEMENT We explore our surroundings by looking at things, but each eye movement that we make causes an abrupt shift of the visual input. Why doesn't the world look like a film recorded on a shaky camera? The answer in part is a brain mechanism called saccadic suppression, which reduces the responses of visual neurons around the time of each eye movement. Here we reveal several new properties of the underlying mechanisms. First, the suppression operates differently in the central and peripheral visual fields. Second, it appears to be controlled by oscillations in the local field potentials at frequencies traditionally associated with attention. These results suggest that saccadic suppression shares the brain circuits responsible for actively ignoring irrelevant stimuli. |
Yan Zhang; Xiaochuan Pan; Rubin Wang; Masamichi Sakagami Functional connectivity between prefrontal cortex and striatum estimated by phase locking value Journal Article In: Cognitive Neurodynamics, vol. 10, no. 3, pp. 245–254, 2016. @article{Zhang2016,The interplay between the prefrontal cortex (PFC) and striatum has an important role in cognitive processes. To investigate interactive functions between the two areas in reward processing, we recorded local field potentials (LFPs) simultaneously from the two areas of two monkeys performing a reward prediction task (large reward vs small reward). The power of the LFPs was calculated in three frequency bands: the beta band (15–29 Hz), the low gamma band (30–49 Hz), and the high gamma band (50–100 Hz). We found that both the PFC and striatum encoded the reward information in the beta band. The reward information was also found in the high gamma band in the PFC, not in the striatum. We further calculated the phase-locking value (PLV) between two LFP signals to measure the phase synchrony between the PFC and striatum. It was found that significant differences occurred between PLVs in different task periods and in different frequency bands. The PLVs in small reward condition were significant higher than that in large reward condition in the beta band. In contrast, the PLVs in the high gamma band were stronger in large reward trials than in small trials. These results suggested that the functional connectivity between the PFC and striatum depended on the task periods and reward conditions. The beta synchrony between the PFC and striatum may regulate behavioral outputs of the monkeys in the small reward condition. |
Huihui Zhou; Robert John Schafer; Robert Desimone Pulvinar-cortex interactions in vision and attention Journal Article In: Neuron, vol. 89, no. 1, pp. 209–220, 2016. @article{Zhou2016c,The ventro-lateral pulvinar is reciprocally connected with the visual areas of the ventral stream that are important for object recognition. To understand the mechanisms of attentive stimulus processing in this pulvinar-cortex loop, we investigated the interactions between the pulvinar, area V4, and IT cortex in a spatial-attention task. Sensory processing and the influence of attention in the pulvinar appeared to reflect its cortical inputs. However, pulvinar deactivation led to a reduction of attentional effects on firing rates and gamma synchrony in V4, a reduction of sensory-evoked responses and overall gamma coherence within V4, and severe behavioral deficits in the affected portion of the visual field. Conversely, pulvinar deactivation caused an increase in low-frequency cortical oscillations, often associated with inattention or sleep. Thus, cortical interactions with the ventro-lateral pulvinar are necessary for normal attention and sensory processing and for maintaining the cortex in an active state. The pulvinar is often proposed to modulate cortical processing with attention. Zhou et al. find that beyond any role in attention, the pulvinar input to cortex seems necessary to maintain the cortex in an active state. |
2015 |
Bram-Ernst Verhoef; Rufin Vogels; Peter Janssen; Leonardo Chelazzi Effects of microstimulation in the anterior intraparietal area during three-dimensional shape categorization Journal Article In: PLoS ONE, vol. 10, no. 8, pp. e0136543, 2015. @article{Verhoef2015,The anterior intraparietal area (AIP) of rhesus monkeys is part of the dorsal visual stream and contains neurons whose visual response properties are commensurate with a role in three-dimensional (3D) shape perception. Neuronal responses in AIP signal the depth structure of disparity-defined 3D shapes, reflect the choices of monkeys while they categorize 3D shapes, and mirror the behavioral variability across different stimulus conditions during 3D-shape categorization. However, direct evidence for a role of AIP in 3D-shape perception has been lacking. We trained rhesus monkeys to categorize disparity-defined 3D shapes and examined AIP's contribution to 3D-shape categorization by microstimulating in clusters of 3D-shape selective AIP neurons during task performance. We find that microstimulation effects on choices (monkey M1) and reaction times (monkey M1 and M2) depend on the 3D-shape preference of the stimulated site. Moreover, electrical stimulation of the same cells, during either the 3D-shape-categorization task or a saccade task, could affect behavior differently. Interestingly, in one monkey we observed a strong correlation between the strength of choice-related AIP activity (choice probabilities) and the influence of microstimulation on 3D-shape-categorization behavior (choices and reaction time). These findings propose AIP as part of the network responsible for 3D-shape perception. The results also show that the anterior intraparietal cortex contains cells with different tuning properties, i.e. 3D-shape- or saccade-related, that can be dynamically read out depending on the requirements of the task at hand. |
Yaoguang Jiang; Dmitry Yampolsky; Gopathy Purushothaman; Vivien A. Casagrande Perceptual decision related activity in the lateral geniculate nucleus Journal Article In: Journal of Neurophysiology, vol. 114, no. 1, pp. 717–735, 2015. @article{Jiang2015,Fundamental to neuroscience is the understanding of how the language of neurons relates to behavior. In the lateral geniculate nucleus (LGN), cells show distinct properties such as selectivity for particular wavelengths, increments or decrements in contrast, or preference for fine detail versus rapid motion. No studies, however, have measured how LGN cells respond when an animal is challenged to make a perceptual decision using information within the receptive fields of those LGN cells. In this study we measured neural activity in the macaque LGN during a two alternative forced choice (2AFC) contrast detection task or during a passive fixation task, and found that a small proportion (13.5%) of single LGN parvocellular (P) and magnocellular (M) neurons matched the psychophysical performance of the monkey. The majority of LGN neurons measured in both tasks were not as sensitive as the monkey. The covariation between neural response and behavior (quantified as choice probability) was significantly above chance during active detection, even when there was no external stimulus. Interneuronal correlations and task-related gain modulations were negligible under the same condition. A bottom-up pooling model that compared sensory neural responses to make perceptual choices in the absence of interneuronal correlations could fully explain these results at the level of the LGN, supporting the hypothesis that the perceptual decision pool consists of multiple sensory neurons, and that response fluctuations in these neurons can influence perception. |
Ken-ichi Amemori; Satoko Amemori; Ann M. Graybiel Motivation and affective judgments differentially recruit neurons in the primate dorsolateral prefrontal and anterior cingulate cortex Journal Article In: Journal of Neuroscience, vol. 35, no. 5, pp. 1939–1953, 2015. @article{Amemori2015a,The judgment of whether to accept or to reject an offer is determined by positive and negative affect related to the offer, but affect also induces motivational responses. Rewarding and aversive cues influence the firing rates of many neurons in primate prefrontal and cingulate neocortical regions, but it still is unclear whether neurons in these regions are related to affective judgment or to motivation.To address this issue, we recorded simultaneously the neuronal spike activities of single units in the dorsolateral prefrontal cortex (dlPFC) and the anterior cingulate cortex (ACC) of macaque monkeys as they performed approach–avoidance (Ap–Av) and approach–approach (Ap–Ap) decision-making tasks that can behaviorally dissociate affective judgment and motivation. Notably, neurons having activity correlated with motivational condition could be distinguished from neurons having activity related to affective judgment, especially in the Ap–Av task. Although many neurons in both regions exhibited similar, selective patterns of task-related activity, we found a larger proportion of neurons activated in low motivational conditions in the dlPFC than in the ACC, and the onset of this activity was signifi- cantly earlier in the dlPFC than in the ACC. Furthermore, the temporal onsets of affective judgment represented by neuronal activities were significantly slower in the low motivational conditions than in the other conditions. These findings suggest that motivation and affective judgment both recruit dlPFC and ACC neurons but with differential degrees of involvement and timing. |
Satoko Amemori; Ken-ichi Amemori; Margaret L. Cantor; Ann M. Graybiel A non-invasive head-holding device for chronic neural recordings in awake behaving monkeys Journal Article In: Journal of Neuroscience Methods, vol. 240, pp. 154–160, 2015. @article{Amemori2015,Background: We have developed a novel head-holding device for behaving non-human primates that affords stability suitable for reliable chronic electrophysiological recording experiments. The device is completely non-invasive, and thus avoids the risk of infection and other complications that can occur with the use of conventional, surgically implanted head-fixation devices. New method: The device consists of a novel non-invasive head mold and bar clamp holder, and is customized to the shape of each monkey's head. The head-holding device that we introduce, combined with our recording system and reflection-based eye-tracking system, allows for chronic behavioral experiments and single-electrode or multi-electrode recording, as well as manipulation of brain activity. Results and comparison with existing methods: With electrodes implanted chronically in multiple brain regions, we could record neural activity from cortical and subcortical structures with stability equal to that recorded with conventional head-post fixation. Consistent with the non-invasive nature of the device, we could record neural signals for more than two years with a single implant. Importantly, the monkeys were able to hold stable eye fixation positions while held by this device, demonstrating the possibility of analyzing eye movement data with only the gentle restraint imposed by the non-invasive head-holding device. Conclusions: We show that the head-holding device introduced here can be extended to the head holding of smaller animals, and note that it could readily be adapted for magnetic resonance brain imaging over extended periods of time. |
Jalal K. Baruni; Brian Lau; C. Daniel Salzman Reward expectation differentially modulates attentional behavior and activity in visual area V4 Journal Article In: Nature Neuroscience, vol. 18, no. 11, pp. 1656–1663, 2015. @article{Baruni2015,Neural activity in visual area V4 is enhanced when attention is directed into neuronal receptive fields. However, the source of this enhancement is unclear, as most physiological studies have manipulated attention by changing the absolute reward associated with a particular location as well as its value relative to other locations. We trained monkeys to discriminate the orientation of two stimuli presented simultaneously in different hemifields while we independently varied the reward magnitude associated with correct discrimination at each location. Behavioral measures of attention were controlled by the relative value of each location. By contrast, neurons in V4 were consistently modulated by absolute reward value, exhibiting increased activity, increased gamma-band power and decreased trial-to-trial variability whenever receptive field locations were associated with large rewards. These data challenge the notion that the perceptual benefits of spatial attention rely on increased signal-to-noise in V4. Instead, these benefits likely derive from downstream selection mechanisms. |
Narcisse P. Bichot; Matthew T. Heard; Ellen M. DeGennaro; Robert Desimone A source for feature-based attention in the prefrontal cortex Journal Article In: Neuron, vol. 88, no. 4, pp. 832–844, 2015. @article{Bichot2015,In cluttered scenes, we can use feature-based attention to quickly locate a target object. To understand how feature attention is used to find and select objects for action, we focused on the ventral prearcuate (VPA) region of prefrontal cortex. In a visual search task, VPA cells responded selectively to search cues, maintained their feature selectivity throughout the delay and subsequent saccades, and discriminated the search target in their receptive fields with a time course earlier than in FEF or IT cortex. Inactivation of VPA impaired the animals' ability to find targets, and simultaneous recordings in FEF revealed that the effects of feature attention were eliminated while leaving the effects of spatial attention in FEF intact. Altogether, the results suggest that VPA neurons compute the locations of objects with the features sought and send this information to FEF to guide eye movements to those relevant stimuli. |
Tommy C. Blanchard; Benjamin Y. Hayden Monkeys are more patient in a foraging task than in a standard intertemporal choice task Journal Article In: PLoS ONE, vol. 10, no. 2, pp. e0117057, 2015. @article{Blanchard2015,Studies of animal impulsivity generally find steep subjective devaluation, or discounting, of delayed rewards - often on the order of a 50% reduction in value in a few seconds. Because such steep discounting is highly disfavored in evolutionary models of time preference, we hypothesize that discounting tasks provide a poor measure of animals' true time preferences. One prediction of this hypothesis is that estimates of time preferences based on these tasks will lack external validity, i.e. fail to predict time preferences in other contexts. We examined choices made by four rhesus monkeys in a computerized patch-leaving foraging task interleaved with a standard intertemporal choice task. Monkeys were significantly more patient in the foraging task than in the intertemporal choice task. Patch-leaving behavior was well fit by parameter-free optimal foraging equations but poorly fit by the hyperbolic discount parameter obtained from the intertemporal choice task. Day-to-day variation in time preferences across the two tasks was uncorrelated with each other. These data are consistent with the conjecture that seemingly impulsive behavior in animals is an artifact of their difficulty understanding the structure of intertemporal choice tasks, and support the idea that animals are more efficient rate maximizers in the multi-second range than intertemporal choice tasks would suggest. |
Tommy C. Blanchard; Caleb E. Strait; Benjamin Y. Hayden Ramping ensemble activity in dorsal anterior cingulate neurons during persistent commitment to a decision Journal Article In: Journal of Neurophysiology, vol. 114, no. 4, pp. 2439–2449, 2015. @article{Blanchard2015a,We frequently need to commit to a choice to achieve our goals; however, the neural processes that keep us motivated in pursuit of delayed goals remain obscure. We examined ensemble responses of neurons in macaque dorsal anterior cingulate cortex (dACC), an area previously implicated in self-control and persistence, in a task that requires commitment to a choice to obtain a reward. After reward receipt, dACC neurons signaled reward amount with characteristic ensemble firing rate patterns; during the delay in anticipation of the reward, ensemble activity smoothly and gradually came to resemble the postreward pattern. On the subset of risky trials, in which a reward was anticipated with 50% certainty, ramping ensemble activity evolved to the pattern associated with the anticipated reward (and not with the anticipated loss) and then, on loss trials, took on an inverted form anticorrelated with the form associated with a win. These findings enrich our knowledge of reward processing in dACC and may have broader implications for our understanding of persistence and self-control. |
Scott L. Brincat; Earl K. Miller Frequency-specific hippocampal-prefrontal interactions during associative learning Journal Article In: Nature Neuroscience, vol. 18, no. 4, pp. 576–581, 2015. @article{Brincat2015,Much of our knowledge of the world depends on learning associations (for example, face-name), for which the hippocampus (HPC) and prefrontal cortex (PFC) are critical. HPC-PFC interactions have rarely been studied in monkeys, whose cognitive and mnemonic abilities are akin to those of humans. We found functional differences and frequency-specific interactions between HPC and PFC of monkeys learning object pair associations, an animal model of human explicit memory. PFC spiking activity reflected learning in parallel with behavioral performance, whereas HPC neurons reflected feedback about whether trial-and-error guesses were correct or incorrect. Theta-band HPC-PFC synchrony was stronger after errors, was driven primarily by PFC to HPC directional influences and decreased with learning. In contrast, alpha/beta-band synchrony was stronger after correct trials, was driven more by HPC and increased with learning. Rapid object associative learning may occur in PFC, whereas HPC may guide neocortical plasticity by signaling success or failure via oscillatory synchrony in different frequency bands. |
Aaron L. Cecala; Ivan Smalianchuk; Sanjeev B. Khanna; Matthew A. Smith; Neeraj J. Gandhi Context cue-dependent saccadic adaptation in rhesus macaques cannot be elicited using color Journal Article In: Journal of Neurophysiology, vol. 114, no. 1, pp. 570–584, 2015. @article{Cecala2015,When the head does not move, rapid movements of the eyes called saccades are used to redirect the line of sight. Saccades are defined by a series of metrical and kinematic (evolution of a movement as a function of time) relationships. For example, the amplitude of a saccade made from one visual target to another is roughly 90% of the distance between the initial fixation point (T0) and the peripheral target (T1). However, this stereotypical relationship between saccade amplitude and initial retinal error (T1-T0) may be altered, either increased or decreased, by surreptitiously displacing a visual target during an ongoing saccade. This form of motor learning (called saccadic adaptation) has been described in both humans and monkeys. Recent experiments in humans and monkeys have suggested that internal (proprioceptive) and external (target shape, color, and/or motion) cues may be used to produce context-dependent adaptation. We tested the hypothesis that an external contextual cue (target color) could be used to evoke differential gain (actual saccade/initial retinal error) states in rhesus monkeys. We did not observe differential gain states correlated with target color regardless of whether targets were displaced along the same vector as the primary saccade or perpendicular to it. Furthermore, this observation held true regardless of whether adaptation trials using various colors and intrasaccade target displacements were randomly intermixed or presented in short or long blocks of trials. These results are consistent with hypotheses that state that color cannot be used as a contextual cue and are interpreted in light of previous studies of saccadic adaptation in both humans and monkeys. |
Jason L. Chan; Michael J. Koval; Thilo Womelsdorf; Stephen G. Lomber; Stefan Everling Dorsolateral prefrontal cortex deactivation in monkeys reduces preparatory beta and gamma power in the superior colliculus Journal Article In: Cerebral Cortex, vol. 25, no. 12, pp. 4704–4714, 2015. @article{Chan2015,Cognitive control requires the selection and maintenance of task-relevant stimulus-response associations, or rules. The dorsolateral prefrontal cortex (DLPFC) has been implicated by lesion, functional imaging, and neurophysiological studies to be involved in encoding rules, but the mechanisms by which it modulates other brain areas are poorly understood. Here, the functional relationship of the DLPFC with the superior colliculus (SC) was investigated by bilaterally deactivating the DLPFC while recording local field potentials (LFPs) in the SC in monkeys performing an interleaved pro- and antisaccade task. Event-related LFPs showed differences between pro- and antisaccades and responded prominently to stimulus presentation. LFP power after stimulus onset was higher for correct saccades than erroneous saccades. Deactivation of the DLPFC did not affect stimulus onset related LFP activity, but reduced high beta (20-30 Hz) and high gamma (60-150 Hz) power during the preparatory period for both pro- and antisaccades. Spike rate during the preparatory period was positively correlated with gamma power and this relationship was attenuated by DLPFC deactivation. These results suggest that top-down control of the SC by the DLPFC may be mediated by beta oscillations. |
Steve W. C. Chang; Nicholas A. Fagan; Koji Toda; Amanda V. Utevsky; John M. Pearson; Michael L. Platt Neural mechanisms of social decision-making in the primate amygdala Journal Article In: Proceedings of the National Academy of Sciences, vol. 112, no. 52, pp. 16012–16017, 2015. @article{Chang2015,SignificanceMaking social decisions requires evaluation of benefits and costs to self and others. Long associated with emotion and vigilance, neurons in primate amygdala also signal reward and punishment as well as information about the faces and eyes of others. Here we show that neurons in the basolateral amygdala signal the value of rewards for self and others when monkeys make social decisions. These value-mirroring neurons reflected monkeys tendency to make prosocial decisions on a momentary as well as long-term basis. We also found that delivering the social peptide oxytocin into basolateral amygdala enhances both prosocial tendencies and attention to the recipients of prosocial decisions. Our findings endorse the amygdala as a critical neural nexus regulating social decisions. Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions. |
Evy Cleeren; Cindy Casteels; Karolien Goffin; Peter Janssen; Wim Van Paesschen Ictal perfusion changes associated with seizure progression in the amygdala kindling model in the rhesus monkey Journal Article In: Epilepsia, vol. 56, no. 9, pp. 1366–1375, 2015. @article{Cleeren2015,OBJECTIVE: Amygdala kindling is a widely used animal model for studying mesial temporal lobe epileptogenesis. In the macaque monkey, electrical amygdala kindling develops slowly and provides an opportunity for investigating ictal perfusion changes during epileptogenesis. METHODS: Two rhesus monkeys were electrically kindled through chronically implanted electrodes in the right amygdala over a period of 16 and 17 months. Ictal perfusion single photon emission computed tomography (SPECT) imaging was performed during each of the four predefined clinical stages. RESULTS: Afterdischarge duration increased slowly over 477 days for monkey K and 515 days for monkey S (18 ± 8 s in stage I; 52 ± 13 s in stage IV). During this time, the animals progressed through four clinical stages ranging from interrupting ongoing behavior to bilateral convulsions. Ictal SPECT perfusion imaging showed well-localized but widely distributed regions of hyperperfusion and hypoperfusion, in both cortical and subcortical structures, at every seizure stage. A large portion of the ictal network was involved in the early stages of epileptogenesis and subsequently expanded over time as seizure severity evolved. SIGNIFICANCE: Our data indicate that the different mesial temporal lobe seizure types occur within a common network affecting several parts of the brain, and that seizure severity may be determined by seizure-induced epileptogenesis within a bihemispheric network that is implicated from the start of the process. |
Victor Lafuente; Mehrdad Jazayeri; Michael N. Shadlen Representation of accumulating evidence for a decision in two parietal areas Journal Article In: Journal of Neuroscience, vol. 35, no. 10, pp. 4306–4318, 2015. @article{Lafuente2015,Decisions are often made by accumulating evidence for and against the alternatives. The momentary evidence represented by sensory neurons is accumulated by downstream structures to form a decision variable, linking the evolving decision to the formation of a motor plan. When decisions are communicated by eye movements, neurons in the lateral intraparietal area (LIP) represent the accumulation of evidence bearing on the potential targets for saccades. We now show that reach-related neurons from the medial intraparietal area (MIP) exhibit a gradual modulation of their firing rates consistent with the representation of an evolving decision variable. When decisions were communicated by saccades instead of reaches, decision-related activity was attenuated in MIP, whereas LIP neurons were active while monkeys communicated decisions by saccades or reaches. Thus, for decisions communicated by a hand movement, a parallel flow of sensory information is directed to parietal areas MIP and LIP during decision formation. |
Caroline B. Drucker; Monica L. Carlson; Koji Toda; Nicholas K. DeWind; Michael L. Platt Non-invasive primate head restraint using thermoplastic masks. Journal Article In: Journal of Neuroscience Methods, vol. 253, pp. 90–100, 2015. @article{Drucker2015,Background: The success of many neuroscientific studies depends upon adequate head fixation of awake, behaving animals. Typically, this is achieved by surgically affixing a head-restraint prosthesis to the skull. New Method: Here we report the use of thermoplastic masks to non-invasively restrain monkeys' heads. Mesh thermoplastic sheets become pliable when heated and can then be molded to an individual monkey's head. After cooling, the custom mask retains this shape indefinitely for day-to-day use. Results: We successfully trained rhesus macaques (Macaca mulatta) to perform cognitive tasks while wearing thermoplastic masks. Using these masks, we achieved a level of head stability sufficient for high-resolution eye-tracking and intracranial electrophysiology. Comparison with Existing Method: Compared with traditional head-posts, we find that thermoplastic masks perform at least as well during infrared eye-tracking and single-neuron recordings, allow for clearer magnetic resonance image acquisition, enable freer placement of a transcranial magnetic stimulation coil, and impose lower financial and time costs on the lab.Conclusions: We conclude that thermoplastic masks are a viable non-invasive form of primate head restraint that enable a wide range of neuroscientific experiments. |
R. Becket Ebitz; Michael L. Platt Neuronal activity in primate dorsal anterior cingulate cortex signals Task conflict and predicts adjustments in pupil-linked arousal Journal Article In: Neuron, vol. 85, no. 3, pp. 628–640, 2015. @article{Ebitz2015,Whether driving a car, shopping for food, or paying attention in a classroom of boisterous teenagers, it's often hard to maintain focus on goals in theface of distraction. Brain imaging studies in humans implicate the dorsal anterior cingulate cortex (dACC) in regulating the conflict between goals and distractors. Here we show that single dACC neurons signal conflict between task goals and distractors in the rhesus macaque, particularly for biologically relevant social stimuli. For some neurons, task conflict signals predicted subsequent changes in pupil size-a peripheral index of arousal linked to noradrenergic tone-associated with reduced distractor interference. dACC neurons also responded to errors, and these signals predicted adjustments in pupil size. These findings provide the first neurophysiological endorsement of the hypothesis that dACC regulates conflict, in part, via modulation of pupil-linked processes such as arousal. |
Samanthi C. Goonetilleke; Leor N. Katz; Daniel K. Wood; Chao Gu; Alexander C. Huk; Brian D. Corneil In: Journal of Neurophysiology, vol. 114, no. 2, pp. 902–913, 2015. @article{Goonetilleke2015,Recent studies have described a phenomenon wherein the onset of a peripheral visual stimulus elicits short-latency (<100 ms) stimulus-locked recruitment (SLR) of neck muscles in nonhuman primates (NHPs), well before any saccadic gaze shift. The SLR is thought to arise from visual responses within the intermediate layers of the superior colliculus (SCi), hence neck muscle recordings may reflect presaccadic activity within the SCi, even in humans. We obtained bilateral intramuscular recordings from splenius capitis (SPL, an ipsilateral head-turning muscle) from 28 human subjects performing leftward or rightward visually guided eye-head gaze shifts. Evidence of an SLR was obtained in 16/55 (29%) of samples; we also observed examples where the SLR was present only unilaterally. We compared these human results with those recorded from a sample of eight NHPs from which recordings of both SPL and deeper suboccipital muscles were available. Using the same criteria, evidence of an SLR was obtained in 8/14 (57%) of SPL recordings, but in 26/29 (90%) of recordings from suboccipital muscles. Thus, both species-specific and muscle- specific factors contribute to the low SLR prevalence in human SPL. Regardless of the presence of the SLR, neck muscle activity in both human SPL and in NHPs became predictive of the reaction time of the ensuing saccade gaze shift ~70 ms after target appearance; such pregaze recruitment likely reflects developing SCi activity, even if the tectoreticulospinal pathway does not reliably relay visually related activity to SPL in humans. |
Chia-Chun Hung; Cecil C. Yen; Jennifer L. Ciuchta; Daniel Papoti; Nicholas A. Bock; David A. Leopold; Afonso C. Silva Functional MRI of visual responses in the awake, behaving marmoset Journal Article In: NeuroImage, vol. 15, no. 120, pp. 1–11, 2015. @article{Hung2015,The visual brain is composed of interconnected subcortical and cortical structures that receive and process image information originating in the retina. The visual system of nonhuman primates, in particular macaques, has been studied in great detail in order to elucidate principles of human sensation and perception. The common marmoset (Callithrix jacchus) is a small New World monkey of growing interest as a primate model for neuroscience. Marmosets have advantages over macaques because of their small size, lissencephalic cortex, and growing potential for viral and genetic manipulations. Previous anatomical studies and electrophysiological recordings in anesthetized marmosets have shown that this species' cortical visual hierarchy closely resembles that of other primates, including humans. Until now, however, there have been no attempts to systematically study visual responses throughout the marmoset brain using fMRI. Here we show that awake marmosets readily learn to carry out a simple visual task inside the bore of an MRI scanner during functional mapping experiments. Functional scanning at 500μm in-plane resolution in a 30 cm horizontal bore at 7T revealed robust positive blood oxygenation level-dependent (BOLD) fMRI responses to visual stimuli throughout visual cortex and associated subcortical areas. Nonvisual sensory areas showed negative contrasts to visual stimuli compared to the fixation dot only baseline. Structured images of objects and faces led to stronger responses than scrambled control images at stages beyond early visual cortex. Our study establishes functionalMRI mapping of visual responses in awake, behaving marmosets is straightforward and valuable for assessing the functional organization of the primate brain at high resolution. |
Chia-Chun Hung; Cecil C. Yen; Jennifer L. Ciuchta; Daniel Papoti; Nicholas A. Bock; David A. Leopold; Afonso C. Silva Functional mapping of face-selective regions in the extrastriate visual cortex of the marmoset Journal Article In: Journal of Neuroscience, vol. 35, no. 3, pp. 1160–1172, 2015. @article{Hung2015a,The cerebral cortex of humans and macaques has specialized regions for processing faces and other visual stimulus categories. It is unknown whether a similar functional organization exists in New World monkeys, such as the common marmoset (Callithrix jacchus), a species of growing interest as a primate model in neuroscience. To address this question, we measured selective neural responses in the brain of four awake marmosets trained to fix their gaze upon images of faces, bodies, objects, and control patterns. In two of the subjects, we measured high gamma-range field potentials from electrocorticography arrays implanted over a large portion of the occipital and inferotemporal cortex. In the other two subjects, we measured BOLD fMRI responses across the entire brain. Both techniques revealed robust, regionally specific patterns of category-selective neural responses. We report that at least six face-selective patches mark the occipitotemporal pathway of the marmoset, with the most anterior patches showing the strongest preference for faces over other stimuli. The similar appearance of these patches to previous findings in macaques and humans, including their apparent arrangement in two parallel pathways, suggests that core elements of the face processing network were present in the common anthropoid primate ancestor living ∼35 million years ago. The findings also identify the marmoset as a viable animal model system for studying specialized neural mechanisms related to high-level social visual perception in humans. |
Ameqrane Ilhame; Wattiez Nicolas; Pouget Pierre; Missal Marcus A subanesthetic dose of ketamine in the Rhesus monkey reduces the occurrence of anticipatory saccades Journal Article In: Psychopharmacology, vol. 232, no. 19, pp. 3563–3572, 2015. @article{Ilhame2015,RATIONALE: It has been shown that antagonism of the glutamatergic N-methyl-D-aspartate (NMDA) receptor with subanesthetic doses of ketamine perturbs the perception of elapsed time. Anticipatory eye movements are based on an internal representation of elapsed time. Therefore, the occurrence of anticipatory saccades could be a particularly sensitive indicator of abnormal time perception due to NMDA receptors blockade. OBJECTIVES: The objective of this study was to determine whether the occurrence of anticipatory saccades could be selectively altered by a subanesthetic dose of ketamine. METHODS: Three Rhesus monkeys were trained in a simple visually guided saccadic task with a variable delay. Monkeys were rewarded for making a visually guided saccade at the end of the delay. Premature anticipatory saccades to the future position of the eccentric target initiated before the end of the delay were not rewarded. A subanesthetic dose of ketamine (0.25 mg/kg) or a saline solution of the same volume was injected i.m. during the task. RESULTS: We found that the injected dose of ketamine did not induce sedation or abnormal behavior. However, in ∼4 min, ketamine induced a strong reduction of the occurrence of anticipatory saccades but did not reduce the occurrence of visually guided saccades. CONCLUSION: This unexpected reduction of anticipatory saccade occurrence could be interpreted as resulting from an altered use of the perception of elapsed time during the delay period induced by NMDA receptors antagonism. |
Mehrdad Jazayeri; Michael N. Shadlen A Neural Mechanism for Sensing and Reproducing a Time Interval Journal Article In: Current Biology, vol. 25, no. 20, pp. 2599–2609, 2015. @article{Jazayeri2015,Timing plays a crucial role in sensorimotor function. However, the neural mechanisms that enable the brain to flexibly measure and reproduce time intervals are not known. We recorded neural activity in parietal cortex of monkeys in a time reproduction task. Monkeys were trained to measure and immediately afterward reproduce different sample intervals. While measuring an interval, neural responses had a nonlinear profile that increased with the duration of the sample interval. Activity was reset during the transition from measurement to production and was followed by a ramping activity whose slope encoded the previously measured sample interval. We found that firing rates at the end of the measurement epoch were correlated with both the slope of the ramp and the monkey's corresponding production interval on a trial-by-trial basis. Analysis of response dynamics further linked the rate of change of firing rates in the measurement epoch to the slope of the ramp in the production epoch. These observations suggest that, during time reproduction, an interval is measured prospectively in relation to the desired motor plan to reproduce that interval. |
Yaoguang Jiang; Gopathy Purushothaman; Vivien A. Casagrande The functional asymmetry of ON and OFF channels in the perception of contrast Journal Article In: Journal of Neurophysiology, vol. 114, pp. 2816–2829, 2015. @article{Jiang2015a,To fully understand the relationship between perception and single neural responses, one should take into consideration the early stages of sensory processing. Few studies, however, have directly examined the neural underpinning of visual perception in the lateral geniculate nucleus (LGN), only one synapse away from the retina. In this study we recorded from LGN parvocellular (P) ON-center and OFF-center neurons while monkeys either passively viewed or actively detected a full range of contrasts. We found that OFF neurons were more sensitive in detecting negative contrasts than ON neurons were in detecting positive contrasts. Also, OFF neurons had higher spontaneous activities, higher peak response amplitudes, and were more sustained than ON neurons in their contrast responses. Puzzlingly, OFF neurons failed to show any significant correlations with the monkeys' perceptual choices, despite their greater contrast sensitivities. If, however, choice probabilities were calculated from interspike intervals instead of spike counts (thus taking into account the higher firing rates of OFF neurons), OFF neurons but not ON neurons were significantly correlated with behavioral choices. Taken together, these results demonstrate in awake, behaving animals that: 1) the ON and OFF pathways do not simply mirror each other in their functionality but instead carry qualitatively different types of information, and 2) the responses of ON and OFF neurons can be correlated with perceptual choices even in the absence of physical stimuli and interneuronal correlations. |
Helen E. Jones; Ian M. Andolina; Stewart D. Shipp; Daniel L. Adams; Javier Cudeiro; Thomas E. Salt; Adam M. Sillito Figure-ground modulation in awake primate thalamus Journal Article In: Proceedings of the National Academy of Sciences, vol. 112, no. 22, pp. 7085–7090, 2015. @article{Jones2015,Figure-ground discrimination refers to the perception of an object, the figure, against a nondescript background. Neural mechanisms of figure-ground detection have been associated with feedback interactions between higher centers and primary visual cortex and have been held to index the effect of global analysis on local feature encoding. Here, in recordings from visual thalamus of alert primates, we demonstrate a robust enhancement of neuronal firing when the figure, as opposed to the ground, component of a motion-defined figure-ground stimulus is located over the receptive field. In this paradigm, visual stimulation of the receptive field and its near environs is identical across both conditions, suggesting the response enhancement reflects higher integrative mechanisms. It thus appears that cortical activity generating the higher-order percept of the figure is simultaneously reentered into the lowest level that is anatomically possible (the thalamus), so that the signature of the evolving representation of the figure is imprinted on the input driving it in an iterative process. |
Paul S. Khayat; Julio C. Martinez-Trujillo Effects of attention and distractor contrast on the responses of middle temporal area neurons to transient motion direction changes Journal Article In: European Journal of Neuroscience, vol. 41, no. 12, pp. 1603–1613, 2015. @article{Khayat2015,The ability of primates to detect transient changes in a visual scene can be influenced by the allocation of attention, as well as by the presence of distractors. We investigated the neural substrates of these effects by recording the responses of neurons in the middle temporal area (MT) of two monkeys while they detected a transient motion direction change in a moving target. We found that positioning a distractor near the target impaired the change-detection performance of the animals. This impairment monotoni- cally decreased as the distractor's contrast decreased. A neural correlate of this effect was a decrease in the ability of MT neu- rons to signal the direction change (detection sensitivity or DS) when a distractor was near the target, both located inside the neuron's receptive field. Moreover, decreasing distractor contrast increased neuronal DS. On the other hand, directing attention away from the target decreased neuronal DS. At the level of individual neurons, we found a negative correlation between the degree of response normalization and the DS. Finally, the intensity of a neuron's response to the change was predictive of the animal's reaction time, suggesting that the activity of our recorded neurons was linked to the animal's detection performance. Our results suggest that the ability of an MT neuron to signal a transient direction change is regulated by the degree of inhibitory drive into the cell. The presence of distractors, their contrast and the allocation of attention influence such inhibitory drive, therefore modulating the ability of the neurons to signal transient changes in stimulus features and consequently behavioral performance. |
Shinichiro Kira; Tianming Yang; Michael N. Shadlen A neural implementation of Wald's Sequential Probability Ratio Test Journal Article In: Neuron, vol. 85, no. 4, pp. 861–873, 2015. @article{Kira2015,Difficult decisions often require evaluation of samples of evidence acquired sequentially. A sensible strategy is to accumulate evidence, weighted by its reliability, until sufficient support is attained. An optimal statistical approach would accumulate evidence in units of logarithms of likelihood ratios (logLR) to a desired level. Studies of perceptual decisions suggest that the brain approximates an analogous procedure, but a direct test of accumulation, in units of logLR, to a threshold in units of cumulative logLR is lacking. We trained rhesus monkeys to make decisions based on a sequence of evanescent, visual cues assigned different logLR, hence different reliability. Firing rates of neurons in the lateral intraparietal area (LIP) reflected the accumulation of logLR and reached a stereotyped level before the monkeys committed to a decision. The monkeys' choices and reaction times, including their variability, were explained by LIP activity in the context of accumulation of logLR to a threshold. |
Thomas Zhihao Luo; John H. R. Maunsell Neuronal modulations in visual cortex are associated with only one of multiple components of attention Journal Article In: Neuron, vol. 86, no. 5, pp. 1182–1188, 2015. @article{Luo2015,Neuronal signals related to visual attention are found in widespread brain regions, and these signals are generally assumed to participate in a common mechanism of attention. However, the behavioral effects of attention in detection can be separated into two distinct components: spatially selective shifts in either the criterion or sensitivity of the subject. Here we show that a paradigm used by many single-neuron studies of attention conflates behavioral changes in the subject's criterion and sensitivity. Then, using a task designed to dissociate these two components, we found that multiple aspects of attention-related neuronal modulations in area V4 of monkey visual cortex corresponded to behavioral shifts in sensitivity, but not criterion. This result suggests that separate components of attention are associated with signals in different brain regions and that attention is not a unitary process in the brain, but instead consists of distinct neurobiological mechanisms. Luo and Maunsell show that the neuronal modulations in visual cortex correspond to only one of multiple components of attention. This result suggests that different brain structures underlie separate mechanisms of attention and that attention is not a unitary process in the brain, but instead consists of distinct neurobiological mechanisms. |
Najib J. Majaj; Ha Hong; Ethan A. Solomon; James J. DiCarlo Simple learned weighted sums of inferior temporal neuronal firing rates accurately predict human core object recognition performance Journal Article In: Journal of Neuroscience, vol. 35, no. 39, pp. 13402–13418, 2015. @article{Majaj2015,To go beyond qualitative models of the biological substrate of object recognition, we ask: can a single ventral stream neuronal linking hypothesis quantitatively account for core object recognition performance over a broad range of tasks? We measured human performance in 64 object recognition tests using thousands ofchallenging images that explore shape similarity and identity preserving object variation. We then used multielectrode arrays to measure neuronal population responses to those same images in visual areas V4 and inferior temporal (IT) cortex ofmonkeys and simulated V1 population responses. We tested leading candidate linking hypotheses and control hypotheses, each postulating how ventral stream neuronal responses underlie object recognition behavior. Specifically, for each hypothesis, we computed the predicted performance on the 64 tests and compared it with the measured pattern ofhuman performance. All tested hypotheses based on low- and mid-level visually evoked activity (pixels, V1, and V4) were very poor predictors ofthe human behavioral pattern. However, simple learned weighted sums of distributed average IT firing rates exactly predicted the behavioral pattern. More elaborate linking hypotheses relying on IT trial-by-trial correlational structure, finer IT temporal codes, or ones that strictly respect the known spatial substructures ofIT (“face patches”) did not improve predictive power. Although these results do not reject those more elaborate hypotheses, they suggest a simple, sufficient quantitative model: each object recognition task is learned from the spatially distributed mean firing rates (100 ms) of ~60,000 IT neurons and is executed as a simple weighted sum ofthose firing rates. |
J. Patrick Mayo; Amie R. DiTomasso; Marc A. Sommer; Matthew A. Smith Dynamics of visual receptive fields in the macaque frontal eye field Journal Article In: Journal of Neurophysiology, vol. 114, no. 6, pp. 3201–3210, 2015. @article{Mayo2015,Neuronal receptive fields (RFs) provide the foundation for understanding systems-level sensory processing. In early visual areas, investigators have mapped RFs in detail using stochastic stimuli and sophisticated analytical approaches. Much less is known about RFs in prefrontal cortex. Visual stimuli used for mapping RFs in prefrontal cortex tend to cover a small range of spatial and temporal parameters, making it difficult to understand their role in visual processing. To address these shortcomings, we implemented a generalized linear model to measure the RFs of neurons in the macaque frontal eye field (FEF) in response to sparse, full-field stimuli. Our high-resolution, probabilistic approach tracked the evolution of RFs during passive fixation, and we validated our results against conventional measures. We found that FEF neurons exhibited a surprising level of sensitivity to stimuli presented as briefly as 10 ms or to multiple dots presented simultaneously, suggesting that FEF visual responses are more precise than previously appreciated. FEF RF spatial structures were largely maintained over time and between stimulus conditions. Our results demonstrate that the application of probabilistic RF mapping to FEF and similar association areas is an important tool for clarifying the neuronal mechanisms of cognition. |
Taihei Ninomiya; Kacie Dougherty; David C. Godlove; Jeffrey D. Schall; Alexander Maier Microcircuitry of agranular frontal cortex: Contrasting laminar connectivity between occipital and frontal areas Journal Article In: Journal of Neurophysiology, vol. 113, no. 9, pp. 3242–3255, 2015. @article{Ninomiya2015,Neocortex is striking in its laminar architecture. Tracer studies have uncovered anatomical connectivity among laminae, but the functional connectivity between laminar compartments is still largely unknown. Such functional connectivity can be discerned through spontaneous neural correlations during rest. Previous work demonstrated a robust pattern of mesoscopic resting-state connectivity in macaque primary visual cortex (V1) through interlaminar cross-frequency coupling. Here we investigated whether this pattern generalizes to other cortical areas by comparing resting-state laminar connectivity between V1 and the supplementary eye field (SEF), a frontal area lacking a granular layer 4 (L4). Local field potentials (LFPs) were recorded with linear microelectrode arrays from all laminae of granular V1 and agranular SEF while monkeys rested in darkness. We found substantial differences in the relationship between the amplitude of gamma-band (>30 Hz) LFP and the phase of alpha-band (7-14 Hz) LFP between these areas. In V1, gamma amplitudes in L2/3 and L5 were coupled with alpha-band LFP phase in L5, as previously described. In contrast, in SEF phase-amplitude coupling was prominent within L3 and much weaker across layers. These results suggest that laminar interactions in agranular SEF are unlike those in granular V1. Thus the intrinsic functional connectivity of the cortical microcircuit does not seem to generalize across cortical areas. |
Shogo Ohmae; Toshimitsu Takahashi; Xiaofeng Lu; Yasunori Nishimori; Yasushi Kodaka; Ichiro Takashima; Shigeru Kitazawa Decoding the timing and target locations of saccadic eye movements from neuronal activity in macaque oculomotor areas Journal Article In: Journal of Neural Engineering, vol. 12, no. 3, pp. 1–21, 2015. @article{Ohmae2015,OBJECTIVE: The control of movement timing has been a significant challenge for brain-machine interfaces (BMIs). As a first step toward developing a timing-based BMI, we aimed to decode movement timing and target locations in a visually guided saccadic eye movement task using the activity of neurons in the primate frontal eye field (FEF) and supplementary eye field (SEF). APPROACH: For this purpose, we developed a template-matching method that could recruit a variety of neurons in these areas. MAIN RESULTS: As a result, we were able to achieve a favorable estimation of saccade onset: for example, data from 20 randomly sampled FEF neurons or 40 SEF neurons achieved a median estimation error of ∼10 ms with an interquartile range less than 50 ms (± ∼25 ms). In the best case, seven simultaneously recorded SEF neurons using a multi-electrode array achieved a comparable accuracy (10 ± 30 ms). The method was significantly better than a heuristic method that used only a group of movement cells with sharp discharges at the onset of saccades. The estimation of target location was less accurate but still favorable, especially when we estimated target location at a timing of 200 ms after the onset of saccade: the method was able to discriminate 16 targets with an accuracy of 90%, which differed not only in their directions (eight directions) but also in amplitude (10/20°) when we used data from 61 randomly sampled FEF neurons. SIGNIFICANCE: The results show that the timing, amplitude and direction of saccades can be decoded from neuronal activity in the FEF and SEF and further suggest that timing-based BMIs can be developed by decoding timing information using the template-matching method. |
Ivo D. Popivanov; Jan Jastorff; Wim Vanduffel; Rufin Vogels Tolerance of macaque middle STS body patch neurons to shape-preserving stimulus transformations Journal Article In: Journal of Cognitive Neuroscience, vol. 27, no. 5, pp. 1001–1016, 2015. @article{Popivanov2015,Functional imaging studies in human and nonhuman primates have demonstrated regions in the brain that show category selectivity for faces or (headless) bodies. Recent fMRI-guided single unit studies of the macaque face category-selective regions have increased our understanding of the response properties of single neurons in these face patches. However, much less is known about the response properties of neurons in the fMRI- defined body category-selective regions (“body patches”). Recently, we reported that the majority of single neurons in one fMRI-defined body patch, the mid-STS body patch, responded more strongly to bodies compared with other objects. Here we assessed the tolerance of these neurons' responses and stimulus preference for shape-preserving image transformations. After mapping the receptive field of the single neurons, we found that their stimulus preference showed a high degree of tolerance for changes in the position and size of the stimulus. However, their response strongly depended on the in-plane orientation of a body. The selectivity ofmost neurons was, to a large degree, preserved when silhouettes were presented instead of the original textured and shaded images, suggesting that mainly shape-based features are driving these neurons. In a human psychophysical study, we showed that the information present in silhouettes is largely sufficient for body versus nonbody categorization. These data suggest that mid-STS body patch neurons respond predominantly to oriented shape features that are prevalent in images of bodies. Their responses can inform position- and retinal size-invariant body categorization and discrimination based on shape. |
M. Victoria Puig; Earl K. Miller Neural substrates of dopamine D2 receptor modulated executive functions in the monkey prefrontal cortex Journal Article In: Cerebral Cortex, vol. 25, no. 9, pp. 2980–2987, 2015. @article{Puig2015,Dopamine D2 receptors (D2R) play a major role in cognition, mood and motor movements. Their blockade by antipsychotic drugs reduces hallucinatory and delusional behaviors in schizophrenia, but often fails to alleviate affective and cognitive dysfunctions. The prefrontal cortex (PFC) expresses D2R and is altered in schizophrenia. We investigated how D2R modulate behavior and PFC function in monkeys. Two monkeys learned new and performed highly familiar visuomotor associations, where each cue was associated with a saccade to a right or left target. We recorded neural spikes and local field potentials from multiple electrodes while injecting the D2R antagonist eticlopride in the lateral PFC. Blocking prefrontal D2R impaired associative learning and cognitive flexibility, reduced motivation, but left the performance of familiar associations intact. Eticlopride reduced saccade-direction selectivity of prefrontal neurons, leading to a decrease in neural information about the associations, and an increase in alpha oscillations. These results, together with our recent study using a D1R antagonist, suggest that D1R and D2R in the primate lateral PFC cooperate to modulate several executive functions. Our findings help to gain insight into why antipsychotic drugs, with strong antagonistic actions on D2R, fail to ameliorate cognitive and emotional deficits in schizophrenia. |
Rishi Rajalingham; Kailyn Schmidt; James J. DiCarlo Comparison of object recognition behavior in human and monkey Journal Article In: Journal of Neuroscience, vol. 35, no. 35, pp. 12127–12136, 2015. @article{rsd15,Although the rhesus monkey is used widely as an animal model of human visual processing, it is not known whether invariant visual object recognition behavior is quantitatively comparable across monkeys and humans. To address this question, we systematically compared the core object recognition behavior of two monkeys with that of human subjects. To test true object recognition behavior (rather than image matching), we generated several thousand naturalistic synthetic images of 24 basic-level objects with high variation in viewing parameters and image background. Monkeys were trained to perform binary object recognition tasks on a match-to-sample paradigm. Data from 605 human subjects performing the same tasks on Mechanical Turk were aggregated to characterize "pooled human" object recognition behavior, as well as 33 separate Mechanical Turk subjects to characterize individual human subject behavior. Our results show that monkeys learn each new object in a few days, after which they not only match mean human performance but show a pattern of object confusion that is highly correlated with pooled human confusion patterns and is statistically indistinguishable from individual human subjects. Importantly, this shared human and monkey pattern of 3D object confusion is not shared with low-level visual representations (pixels, V1+; models of the retina and primary visual cortex) but is shared with a state-of-the-art computer vision feature representation. Together, these results are consistent with the hypothesis that rhesus monkeys and humans share a common neural shape representation that directly supports object perception. |
Supriya Ray; Stephen J. Heinen A mechanism for decision rule discrimination by supplementary eye field neurons Journal Article In: Experimental Brain Research, vol. 233, no. 2, pp. 459–476, 2015. @article{rh15,A decision to select an action from alternatives is often guided by rules that flexibly map sensory inputs to motor outputs when certain conditions are satisfied. However, the neural mechanisms underlying rule-based decision making remain poorly understood. Two complementary types of neurons in the supplementary eye field (SEF) of macaques have been identified that modulate activity differentially to interpret rules in an ocular go–nogo task, which stipulates that the animal either visually pursue a moving object if it intersects a visible zone (‘go'), or maintain fixation if it does not (‘nogo'). These neurons discriminate between go and nogo rule-states by increasing activity to signal their preferred (agonist) rule-state and decreasing activity to signal their non-preferred (antagonist) rule-state. In the current study, we found that SEF neurons decrease activity in anticipation of the antagonist rule-state, and do so more rapidly when the rule-state is easier to predict. This rapid decrease in activity could underlie a process of elimination in which trajectories that do not invoke the preferred rule-state receive no further computational resources. Furthermore, discrimination between difficult and easy trials in the antagonist rule-state occurs prior to when discrimination within the agonist rule-state occurs. A winner-take-all like model that incorporates a pair of mutually inhibited integrators to accumulate evidence in favor of either the decision to pursue or the decision to continue fixation accounts for the observed neural phenomena. |
