Non-Human Primate Eye-Tracking Publications
All EyeLink eye tracker non-human primate research publications up until 2024 (with some early 2025s) are listed below by year. You can search the eye-tracking publications using keywords such as Temporal Cortex, Macaque, Antisaccade, etc. You can also search for individual author names. If we missed any EyeLink non-human primate articles, please email us!
2017 |
Aishwarya Parthasarathy; Roger Herikstad; Jit Hon Bong; Felipe Salvador Medina; Camilo Libedinsky; Shih-Cheng Yen Mixed selectivity morphs population codes in prefrontal cortex Journal Article In: Nature Neuroscience, vol. 20, no. 12, pp. 1770–1779, 2017. @article{Parthasarathy2017,The prefrontal cortex plays an important role in the maintenance of working memory, as evidenced by studies using microelectrode recordings 1, lesions 2, inactivation 3, micro-stimulation 4, 5, and functional neuroimaging 6. Furthermore, the pre-frontal cortex suppresses task-irrelevant stimuli, or distractors 3, 7, 8. This has led to the notion that the prefrontal cortex plays a central role in the maintenance of working memory and the suppression of distractors, which are cornerstones of executive processing. Individual neurons in the lateral prefrontal cortex (LPFC; Brodmann area 46) show selective, sustained activity during the delay period of working memory and only as long as the memory is maintained 1,9,10. Populations of LPFC neurons form a stable memory code during the delay period of a working memory task 11. Distractors are thought to be suppressed in the LPFC, since it responds less to distractors than to task-relevant stimuli 3, 7, 8. Notably, sustained activity of LPFC neurons persists even after distractors are presented 3, 10. Thus, it is reasonable to hypothesize that the stable code observed during the delay period persists after a distractor is presented, forming a persistent code throughout the memory period. Recent studies have shown that the LPFC hosts an abundance of neurons with mixed selectivity 12-19. These cells encode multiple parameters of the task simultaneously, such as sensory stimuli, task rule, or motor response. In particular, neurons with nonlinear mixed selectivity (NMS) are thought to play a key role in the encoding of information 18, 20. In the context of a working memory task with interfering distractors, mixed selectivity could lead to a change in code after the distractor is presented. Thus, it is also reasonable to hypothesize that the code does not persist throughout the memory period but rather that it is flexible, with the ability to adapt to new task contingencies, such as the presentation of a distractor. Here we found that the LPFC morphs its code, as the latter hypothesis predicts , while the frontal eye fields (FEF) maintain a stable code, in agreement with the former hypothesis. Results Two monkeys were trained to perform a delayed saccade task (Fig. 1a). Overall performance of both animals was higher than 75% correct (Fig. 1b). We recorded a total of 256 neurons from the LPFC (144 from Monkey A and 112 from Monkey B; the positions of the implanted electrode arrays are shown in red in Fig. 1c) and 137 neurons from the FEF (125 from Monkey A and 12 from Monkey B; electrode arrays are shown in blue in Fig. 1c) while the animals performed the task. Of the neurons recorded, more than 40% displayed selectiv-ity to target location in at least one stage during the trial (Fig. 1d). Examples of the responses of an LPFC and an FEF neuron are shown in Supplementary Fig. 1a,b. To quantify the magnitude of this selec-tivity, we computed the percentage of explained variance (PEV) for spatial selectivity in each neuron. The average PEVs across significant neurons (Methods) are shown in Fig. 1d. In the LPFC, we observed that target information in selective cells (n = 107, 42% of the LPFC population) increased during the target presentation period and remained stable throughout the rest of the trial (Fig. 1d). In addition, in Supplementary Fig. 1c, we show that the distractor information was much lower in these same neurons during the Delay 2 period (P < 0.001, Hedges' g = 23.99). A previous study found a sharp decrease in target information following distractor presentation , together with an increase of distractor information 21. Our results, however, did not replicate these observations. Rather, we found that target information remained stable, and distractor information stayed close to baseline throughout the trial (Supplementary Fig. 1c). This difference may reflect the simpler nature of our task and the comparatively lower behavioral saliency of the distractor we used. It may also reflect differences in the ways different types of information are encoded; perhaps the working memory code for numerosity in LPFC is more susceptible to distractors than the code for spatial locations. In contrast, in the FEF we observed The prefrontal cortex maintains working memory information in the presence of distracting stimuli. It has long been thought that sustained activity in individual neurons or groups of neurons was responsible for maintaining information in the form of a persistent, stable code. Here we show that, upon the presentation of a distractor, information in the lateral prefrontal cortex was reorganized into a different pattern of activity to create a morphed stable code without losing information. In contrast, the code in the frontal eye fields persisted across different delay periods but exhibited substantial instability and information loss after the presentation of a distractor. We found that neurons with mixed-selective responses were necessary and sufficient for the morphing of code and that these neurons were more abundant in the lateral prefrontal cortex than the frontal eye fields. This suggests that mixed selectivity provides populations with code-morphing capability, a property that may underlie cognitive flexibility. |
Tyler R. Peel; Suryadeep Dash; Stephen G. Lomber; Brian D. Corneil Frontal eye field inactivation diminishes superior colliculus activity, but delayed saccadic accumulation governs reaction time increases Journal Article In: Journal of Neuroscience, vol. 37, no. 48, pp. 11715–11730, 2017. @article{Peel2017,Stochastic accumulator models provide a comprehensive framework for how neural activity could produce behavior. Neural activity within the frontal eye fields (FEFs) and intermediate layers of the superior colliculus (iSC) support such models for saccade initiation by relating variations in saccade reaction time (SRT) to variations in such parameters as baseline, rate of accumulation of activity, and threshold. Here, by recording iSC activity during reversible cryogenic inactivation of the FEF in four male nonhuman primates, we causally tested which parameter(s) best explains concomitant increases in SRT. While FEF inactivation decreased all aspects of ipsilesional iSC activity, decreases in accumulation rate and threshold poorly predicted accompanying increases in SRT. Instead, SRT increases best correlated with delays in the onset of saccade-related accumulation. We conclude that FEF signals govern the onset of saccade-related accumulation within the iSC, and that the onset of accumulation is a relevant parameter for stochastic accumulation models of saccade initiation. |
Joel Reithler; Judith C. Peters; Rainer Goebel In: NeuroImage, vol. 152, pp. 551–562, 2017. @article{Reithler2017,Visual scenes are initially processed via segregated neural pathways dedicated to either of the two visual hemifields. Although higher-order visual areas are generally believed to utilize invariant object representations (abstracted away from features such as stimulus position), recent findings suggest they retain more spatial information than previously thought. Here, we assessed the nature of such higher-order object representations in human cortex using high-resolution fMRI at 7T, supported by corroborative 3T data. We show that multi-voxel activation patterns in both the contra- and ipsilateral hemisphere can be exploited to successfully classify the object category of unilaterally presented stimuli. Moreover, robustly identified rank order-based response profiles demonstrated a strong contralateral bias which frequently outweighed object category preferences. Finally, we contrasted different combinatorial operations to predict the responses during bilateral stimulation conditions based on responses to their constituent unilateral elements. Results favored a max operation predominantly reflecting the contralateral stimuli. The current findings extend previous work by showing that configuration-dependent modulations in higher-order visual cortex responses as observed in single unit activity have a counterpart in human neural population coding. They furthermore corroborate the emerging view that position coding is a fundamental functional characteristic of ventral visual stream processing. |
Douglas A. Ruff; Marlene R. Cohen A normalization model suggests that attention changes the weighting of inputs between visual areas Journal Article In: Proceedings of the National Academy of Sciences, vol. 114, no. 20, pp. E4085–E4094, 2017. @article{Ruff2017,Models of divisive normalization can explain the trial-averaged responses of neurons in sensory, association, and motor areas under a wide range of conditions, including how visual attention changes the gains of neurons in visual cortex. Attention, like other modulatory processes, is also associated with changes in the extent to which pairs of neurons share trial-to-trial variability. We showed recently that in addition to decreasing correlations between similarly tuned neurons within the same visual area, attention increases correlations between neurons in primary visual cortex (V1) and the middle temporal area (MT) and that an extension of a classic normalization model can account for this correlation increase. One of the benefits of having a descriptive model that can account for many physiological observations is that it can be used to probe the mechanisms underlying processes such as attention. Here, we use electrical microstimulation in V1 paired with recording in MT to provide causal evidence that the relationship between V1 and MT activity is nonlinear and is well described by divisive normalization. We then use the normalization model and recording and microstimulation experiments to show that the attention dependence of V1-MT correlations is better explained by a mechanism in which attention changes the weights of connections between V1 and MT than by a mechanism that modulates responses in either area. Our study shows that normalization can explain interactions between neurons in different areas and provides a framework for using multiarea recording and stimulation to probe the neural mechanisms underlying neuronal computations. |
Aldo Rustichini; Katherine E. Conen; Xinying Cai; Camillo Padoa-Schioppa Optimal coding and neuronal adaptation in economic decisions Journal Article In: Nature Communications, vol. 8, pp. 1208, 2017. @article{Rustichini2017,During economic decisions, offer value cells in orbitofrontal cortex (OFC) encode the values of offered goods. Furthermore, their tuning functions adapt to the range of values available in any given context. A fundamental and open question is whether range adaptation is behaviorally advantageous. Here we present a theory of optimal coding for economic decisions. We propose that the representation of offer values is optimal if it ensures maximal expected payoff. In this framework, we examine offer value cells in non-human primates. We show that their responses are quasi-linear even when optimal tuning functions are highly non-linear. Most importantly, we demonstrate that for linear tuning functions range adaptation maximizes the expected payoff. Thus value coding in OFC is functionally rigid (linear tuning) but parametrically plastic (range adaptation with optimal gain). Importantly, the benefit of range adaptation outweighs the cost of functional rigidity. While generally suboptimal, linear tuning may facilitate transitive choices. |
Philipp Schwedhelm; Daniel Baldauf; Stefan Treue Electrical stimulation of macaque lateral prefrontal cortex modulates oculomotor behavior indicative of a disruption of top-down attention Journal Article In: Scientific Reports, vol. 7, pp. 17715, 2017. @article{Schwedhelm2017,The lateral prefrontal cortex (lPFC) of primates is hypothesized to be heavily involved in decision-making and selective visual attention. Recent neurophysiological evidence suggests that information necessary for an orchestration of those high-level cognitive factors are indeed represented in the lPFC. However, we know little about the specific contribution of sub-networks within lPFC to the deployment of top-down influences that can be measured in extrastriate visual cortex. Here, we systematically applied electrical stimulations to areas 8Av and 45 of two macaque monkeys performing a concurrent goal-directed saccade task. Despite using currents well above saccadic thresholds of the directly adjacent Frontal Eye Fields (FEF), saccades were only rarely evoked by the stimulation. Instead, two types of behavioral effects were observed: Stimulations of caudal sites in 8Av (close to FEF) shortened or prolonged saccadic reaction times, depending on the task-instructed saccade, while rostral stimulations of 8Av/45 seem to affect the relative attentional weighting of saccade targets as well as saccadic reaction times. These results illuminate important differences in the causal involvement of different sub-networks within the lPFC and are most compatible with a stimulation-induced biasing of stimulus processing that accelerates the detection of saccade targets presented ipsilateral to stimulation through a disruption of contralaterally deployed top-down attention. |
Lenka Seillier; Corinna Lorenz; Katsuhisa Kawaguchi; Torben Ott; Andreas Nieder; Paria Pourriahi; Hendrikje Nienborg Serotonin decreases the gain of visual responses in awake macaque V1 Journal Article In: Journal of Neuroscience, vol. 37, no. 47, pp. 11390 –11405 Systems/Circuits, 2017. @article{Seillier2017,Serotonin, an important neuromodulator in the brain, is implicated in affective and cognitive functions. However, its role even for basic cortical processes is controversial. For example, in the mammalian primary visual cortex (V1), heterogenous serotonergic modulation has been observed in anesthetized animals. Here, we combined extracellular single-unit recordings with iontophoresis in awake animals. We examined the role of serotonin on well-defined tuning properties (orientation, spatial frequency, contrast, and size) in V1 of two male macaque monkeys. We find that in the awake macaque the modulatory effect of serotonin is surprisingly uniform: it causes a mainly multiplicative decrease of the visual responses and a slight increase in the stimulus-selective response latency. Moreover, serotonin neither systematically changes the selectivity or variability of the response, nor the interneuronal correlation unexplained by the stimulus ("noise-correlation"). The modulation by serotonin has qualitative similarities with that for a decrease in stimulus contrast, but differs quantitatively from decreasing contrast. It can be captured by a simple additive change to a threshold-linear spiking nonlinearity. Together, our results show that serotonin is well suited to control the response gain of neurons in V1 depending on the animal's behavioral or motivational context, complementing other known state-dependent gain-control mechanisms. |
Brianna J. Sleezer; Giuliana A. LoConte; Meghan D. Castagno; Benjamin Y. Hayden Neuronal responses support a role for orbitofrontal cortex in cognitive set reconfiguration Journal Article In: European Journal of Neuroscience, vol. 45, pp. 940–951, 2017. @article{Sleezer2017,We are often faced with the need to abandon no-longer beneficial rules and adopt new ones. This process, known as cognitive set reconfiguration, is a hallmark of executive control. Although cognitive functions like reconfiguration are most often associated with dorsal prefrontal structures, recent evidence suggests that the orbitofrontal cortex (OFC) may play an important role as well. We recorded the activity of OFC neurons while rhesus macaques performed an analogue of the Wisconsin Card Sorting Task that involved a trial and error stage. The OFC neurons demonstrated two types of switch-related activity, an early (switch-away) signal and a late (switch-to) signal, when the new task set was established. We also found a pattern of match modulation: a sig- nificant change in activity for the stimulus that matched the current perceptual rule (and would therefore be selected). These results extend our understanding of the executive functions of the OFC. They also allow us to directly compare the OFC with the complementary datasets we previously collected in the ventral (VS) and dorsal (DS) striatum. Although both effects are observed in all three areas, the timing of responses aligns the OFC more closely with DS than with VS. |
Courtney Turrin; Nicholas A. Fagan; Olga Dal Monte; Steve W. C. Chang Social resource foraging is guided by the principles of the Marginal Value Theorem Journal Article In: Scientific Reports, vol. 7, pp. 11274, 2017. @article{Turrin2017,Optimality principles guide how animals adapt to changing environments. During foraging for nonsocial resources such as food and water, species across taxa obey a strategy that maximizes resource harvest rate. However, it remains unknown whether foraging for social resources also obeys such a strategic principle. We investigated how primates forage for social information conveyed by conspecific facial expressions using the framework of optimal foraging theory. We found that the canonical principle of Marginal Value Theorem (MVT) also applies to social resources. Consistent with MVT, rhesus macaques (Macaca mulatta) spent more time foraging for social information when alternative sources of information were farther away compared to when they were closer by. A comparison of four models of patch-leaving behavior confirmed that the MVT framework provided the best fit to the observed foraging behavior. This analysis further demonstrated that patch-leaving decisions were not driven simply by the declining value of the images in the patch, but instead were dependent upon both the instantaneous social value intake rate and current time in the patch. |
Jordi Aguila; F. Javier Cudeiro; Casto Rivadulla In: Cerebral Cortex, vol. 27, no. 6, pp. 3331–3345, 2017. @article{Aguila2017,In awake monkeys, we used repetitive transcranial magnetic stimulation (rTMS) to focally inactivate visual cortex while measuring the responsiveness of parvocellular lateral geniculate nucleus (LGN) neurons. Effects were noted in 64/75 neurons, and could be divided into 2 main groups: (1) for 39 neurons, visual responsiveness decreased and visual latency increased without apparent shift in receptive field (RF) position and (2) a second group (n = 25, 33% of the recorded cells) whose excitability was not compromised, but whose RF position shifted an average of 4.5°. This change is related to the retinotopic correspondence observed between the recorded thalamic area and the affected cortical zone. The effect of inactivation for this group of neurons was compatible with silencing the original retinal drive and unmasking a second latent retinal drive onto the studied neuron. These results indicate novel and remarkable dynamics in thalamocortical circuitry that force us to reassess constraints on retinogeniculate transmission. |
Habiba Azab; Benjamin Y. Hayden Correlates of decisional dynamics in the dorsal anterior cingulate cortex Journal Article In: PLoS Biology, vol. 15, no. 11, pp. e2003091, 2017. @article{Azab2017,We hypothesized that during binary economic choice, decision makers use the first option they attend as a default to which they compare the second. To test this idea, we recorded activity of neurons in the dorsal anterior cingulate cortex (dACC) of macaques choosing between gambles presented asynchronously. We find that ensemble encoding of the value of the first offer includes both choice-dependent and choice-independent aspects, as if reflecting a partial decision. That is, its responses are neither entirely pre- nor post-decisional. In contrast, coding of the value of the second offer is entirely decision dependent (i.e., post-decisional). This result holds even when offer-value encodings are compared within the same time period. Additionally, we see no evidence for 2 pools of neurons linked to the 2 offers; instead, all comparison appears to occur within a single functionally homogenous pool of task-selective neurons. These observations suggest that economic choices reflect a context-dependent evaluation of attended options. Moreover, they raise the possibility that value representations reflect, to some extent, a tentative commitment to a choice. |
Sahand Babapoor-Farrokhran; Martin Vinck; Thilo Womelsdorf; Stefan Everling Theta and beta synchrony coordinate frontal eye fields and anterior cingulate cortex during sensorimotor mapping Journal Article In: Nature Communications, vol. 8, pp. 13967, 2017. @article{BabapoorFarrokhran2017,The frontal eye fields (FEFs) and the anterior cingulate cortex (ACC) are commonly coacti- vated for cognitive saccade tasks, but whether this joined activation indexes coordinated activity underlying successful guidance of sensorimotor mapping is unknown. Here we test whether ACC and FEF circuits coordinate through phase synchronization of local field potential and neural spiking activity in macaque monkeys performing memory-guided and pro- and anti-saccades. We find that FEF and ACC showed prominent synchronization at a 3–9 Hz theta and a 12–30 Hz beta frequency band during the delay and preparation periods with a strong Granger-causal influence from ACC to FEF. The strength of theta- and beta- band coherence between ACC and FEF but not variations in power predict correct task performance. Taken together, the results support a role of ACC in cognitive control of fron- toparietal networks and suggest that narrow-band theta and to some extent beta rhythmic activity indexes the coordination of relevant information during periods of enhanced control demands. |
David L. Barack; Steve W. C. Chang; Michael L. Platt Posterior cingulate neurons dynamically signal decisions to disengage during foraging Journal Article In: Neuron, vol. 96, no. 2, pp. 339–347.e5, 2017. @article{Barack2017,Foraging for resources is a fundamental behavior balancing systematic search and strategic disengagement. The foraging behavior of primates is especially complex and requires long-term memory, value comparison, strategic planning, and decision-making. Here we provide evidence from two different foraging tasks that neurons in primate posterior cingulate cortex (PCC) signal decision salience during foraging to motivate disengagement from the current strategy. In our foraging tasks, salience refers to the difference between decision thresholds and the net harvested reward. Salience signals were stronger in poor foraging contexts than rich ones, suggesting low harvest rates recruit mechanisms in PCC that regulate strategic disengagement and exploration during foraging. Barack et al. report that foraging salience motivated strategic disengagement in two distinct tasks. Posterior cingulate neurons preferentially signaled salience and forecast divergent choices when reward rates were low, suggesting a role in the strategic control of behavior. |
Charles B. Beaman; Sarah L. Eagleman; Valentin Dragoi Sensory coding accuracy and perceptual performance are improved during the desynchronized cortical state Journal Article In: Nature Communications, vol. 8, pp. 1308, 2017. @article{Beaman2017,Cortical activity changes continuously during the course of the day. At a global scale, population activity varies between the ‘synchronized' state during sleep and ‘desynchronized' state during waking. However, whether local fluctuations in population synchrony during wakefulness modulate the accuracy of sensory encoding and behavioral performance is poorly understood. Here, we show that populations of cells in monkey visual cortex exhibit rapid fluctuations in synchrony ranging from desynchronized responses, indicative of high alertness, to highly synchronized responses. These fluctuations are local and control the trial variability in population coding accuracy and behavioral performance in a discrimination task. When local population activity is desynchronized, the correlated variability between neurons is reduced, and network and behavioral performance are enhanced. These findings demonstrate that the structure of variability in local cortical populations is not noise but rather controls how sensory information is optimally integrated with ongoing processes to guide network coding and behavior. |
Joachim Bellet; Chih-Yang Chen; Ziad M. Hafed Sequential hemifield gating of alpha and beta behavioral performance oscillations after microsaccades Journal Article In: Journal of Neurophysiology, vol. 118, pp. 2789–2805, 2017. @article{Bellet2017,Microsaccades are tiny saccades that occur during gaze fixation. Even though visual processing has been shown to be strongly modulated close to the time of microsaccades, both at central and peripheral eccentricities, it is not clear how these eye movements might influence longer term fluctuations in brain activity and behavior. Here we found that visual processing is significantly affected and, in a rhythmic manner, even several hundreds of milliseconds after a microsaccade. Human visual detection efficiency, as measured by reaction time, exhibited coherent rhythmic oscillations in the ? - and ? -frequency bands for up to ~650–700 ms after a microsaccade. Surprisingly, the oscillations were sequentially pulsed across visual hemifields relative to microsaccade direction, first occurring in the same hemifield as the movement vector for ~400 ms and then the opposite. Such pulsing also affected perceptual detection performance. Our results suggest that visual processing is subject to long-lasting oscillations that are phase locked to microsaccade generation, and that these oscillations are dependent on microsaccade direction. |
Kelly R. Bullock; Florian Pieper; Adam J. Sachs; Julio C. Martinez-Trujillo Visual and presaccadic activity in area 8Ar of the macaque monkey lateral prefrontal cortex Journal Article In: Journal of Neurophysiology, vol. 118, no. 1, pp. 15–28, 2017. @article{Bullock2017,Common trends observed in many visual and oculomotor-related cortical areas include retinotopically organized receptive and movement fields exhibiting a Gaussian shape and increasing size with eccentricity. These trends are demonstrated in the frontal eye fields (FEF), many visual areas, and the superior colliculus (SC), but have not been thoroughly characterized in prearcuate area 8Ar of the prefrontal cortex. This is important since area 8Ar, located anterior to the FEF, is more cytoarchitectonically similar to prefrontal areas than premotor areas. Here we recorded the responses of 166 neurons in area 8Ar of two male macaques while the animals made visually guided saccades to a peripheral sine-wave grating stimulus positioned at one of 40 possible locations (8 angles along 5 eccentricities). To characterize the neurons' receptive and movement fields, we fit a bivariate Gaussian model to the baseline-subtracted average firing rate during stimulus presentation (early and late visual epoch) and prior to saccade onset (presaccadic epoch). 121/166 neurons showed spatially selective visual and presaccadic responses. Of the visually selective neurons, 76% preferred the contralateral visual hemifield, whereas 24% preferred the ipsilateral hemifield. The angular width of visual and movement-related fields scaled positively with increasing eccentricity. Moreover, responses of neurons with visual receptive fields were modulated by target contrast exhibiting sigmoid tuning curves that resemble those of visual neurons in upstream areas such as MT and V4. Finally, we found that neurons with receptive fields at similar spatial locations were clustered within the area; however, this organization did not appear retinotopic. |
Jason L. Chan; Michael J. Koval; Kevin D. Johnston; Stefan Everling Neural correlates for task switching in the macaque superior colliculus Journal Article In: Journal of Neurophysiology, vol. 118, pp. 2156–2170, 2017. @article{Chan2017,Successful task switching requires a network of brain areas to select, maintain, implement, and execute the appropriate task. Although frontoparietal brain areas are thought to play a critical role in task switching by selecting and encoding task rules and exerting top-down control, how brain areas closer to the execution of tasks participate in task switching is unclear. The superior colliculus (SC) integrates information from various brain areas to generate saccades and is likely influenced by task switching. Here, we investigated switch costs in nonhuman primates and their neural correlates in the activity of SC saccade-related neurons in monkeys performing cued, randomly interleaved pro- and anti-saccade trials. We predicted that behavioral switch costs would be associated with differential modulations of SC activity in trials on which the task was switched vs. repeated, with activity on the current trial resembling that associated with the task set of the previous trial when a switch occurred. We observed both error rate and reaction time switch costs and changes in the discharge rate and timing of activity in SC neurons between switch and repeat trials. These changes were present later in the task only after fixation on the cue stimuli but before saccade onset. These results further establish switch costs in macaque monkeys and suggest that SC activity is modulated by task-switching processes in a manner inconsistent with the concept of task set inertia. |
Benjamin W. Corrigan; Roberto A. Gulli; Guillaume Doucet; Julio C. Martinez-Trujillo Characterizing eye movement behaviors and kinematics of non-human primates during virtual navigation tasks Journal Article In: Journal of Vision, vol. 17, no. 12, pp. 1–22, 2017. @article{Corrigan2017,Virtual environments (VE) allow testing complex behaviors in naturalistic settings by combining highly controlled visual stimuli with spatial navigation and other cognitive tasks. They also allow for the recording of eye movements using high-precision eye tracking techniques, which is important in electrophysiological studies examining the response properties of neurons in visual areas of nonhuman primates. However, during virtual navigation, the pattern of retinal stimulation can be highly dynamic which may influence eye movements. Here we examine whether and how eye movement patterns change as a function of dynamic visual stimulation during virtual navigation tasks, relative to standard oculomotor tasks. We trained two rhesus macaques to use a joystick to navigate in a VE to complete two tasks. To contrast VE behavior with classic measurements, the monkeys also performed a simple Cued Saccade task. We used a robust algorithm for rapid classification of saccades, fixations, and smooth pursuits. We then analyzed the kinematics of saccades during all tasks, and specifically during different phases of the VE tasks. We found that fixation to smooth pursuit ratios were smaller in VE tasks (4:5) compared to the Cued Saccade task (7:1), reflecting a more intensive use of smooth pursuit to foveate targets in VE than in a standard visually guided saccade task or during spontaneous fixations. Saccades made to rewarded targets (exploitation) tended to have increased peak velocities compared to saccades made to unrewarded objects (exploration). VE exploitation saccades were 6% slower than saccades to discrete targets in the Cued Saccade task. Virtual environments represent a technological advance in experimental design for nonhuman primates. Here we provide a framework to study the ways that eye movements change between and within static and dynamic displays. |
Nan Jia; Scott L. Brincat; Andrés F. Salazar-Gómez; Mikhail Panko; Frank H. Guenther; Earl K. Miller Decoding of intended saccade direction in an oculomotor brain-computer interface Journal Article In: Journal of Neural Engineering, vol. 14, no. 4, pp. 1–13, 2017. @article{Jia2017a,OBJECTIVE: To date, invasive brain-computer interface (BCI) research has largely focused on replacing lost limb functions using signals from of hand/arm areas of motor cortex. However, the oculomotor system may be better suited to BCI applications involving rapid serial selection from spatial targets, such as choosing from a set of possible words displayed on a computer screen in an augmentative and alternative communication (AAC) application. Here we aimed to demonstrate the feasibility of a BCI utilizing the oculomotor system. APPROACH: We developed a chronic intracortical BCI in monkeys to decode intended saccadic eye movement direction using activity from multiple frontal cortical areas. MAIN RESULTS: Intended saccade direction could be decoded in real time with high accuracy, particularly at contralateral locations. Accurate decoding was evident even at the beginning of the BCI session; no extensive BCI experience was necessary. High-frequency (80-500 Hz) local field potential magnitude provided the best performance, even over spiking activity, thus simplifying future BCI applications. Most of the information came from the frontal and supplementary eye fields, with relatively little contribution from dorsolateral prefrontal cortex. SIGNIFICANCE: Our results support the feasibility of high-accuracy intracortical oculomotor BCIs that require little or no practice to operate and may be ideally suited for 'point and click' computer operation as used in most current AAC systems. |
Yoshinao Kajikawa; John F. Smiley; Charles E. Schroeder Primary generators of visually evoked field potentials recorded in the macaque auditory cortex Journal Article In: Journal of Neuroscience, vol. 37, no. 42, pp. 10139–10153, 2017. @article{Kajikawa2017,Prior studies have reported “local” field potential (LFP) responses to faces in the macaque auditory cortex and have suggested that such face-LFPs may be substrates of audiovisual integration. However, although field potentials (FPs) may reflect the synaptic currents of neurons near the recording electrode, due to the use of a distant reference electrode, they often reflect those of synaptic activity occurring in distant sites as well. Thus, FP recordings within a given brain region (e.g., auditory cortex) may be “contaminated” by activity generated elsewhere in the brain. To determine whether face responses are indeed generated within macaque auditory cortex, we recorded FPs and concomitant multiunit activity with linear array multielectrodes across auditory cortex in three macaques (one female), and applied current source density (CSD) analysis to the laminar FP profile. CSD analysis revealed no appreciable local generator contribution to the visual FP in auditory cortex, although we did note an increase in the amplitude of visual FP with cortical depth, suggesting that their generators are located below auditory cortex. In the underlying inferotemporal cortex, we found polarity inversions of the main visual FP components accompanied by robust CSD responses and large-amplitude multiunit activity. These results indicate that face-evoked FP responses in auditory cortex are not generated locally but are volume-conducted from other face-responsive regions. In broader terms, our results underscore the caution that, unless far-field contamination is removed, LFPs in general may reflect such “far-field” activity, in addition to, or in absence of, local synaptic responses. |
Kohitij Kar; Jacob Duijnhouwer; Bart Krekelberg Transcranial alternating current stimulation attenuates neuronal adaptation Journal Article In: Journal of Neuroscience, vol. 37, no. 9, pp. 2325–2335, 2017. @article{Kar2017,We previously showed that brief application of 2 mA (peak-to-peak) transcranial currents alternating at 10 Hz significantly reduces motion adaptation in humans. This is but one of many behavioral studies showing that weak currents applied to the scalp modulate neural processing. Transcranial stimulation has been shown to improve perception, learning, and a range of clinical symptoms. Few studies, however, have measured the neural consequences of transcranial current stimulation. We capitalized on the strong link between motion perception and neural activity in the middle temporal (MT) area of the macaque monkey to study the neural mechanisms that underlie the behavioral consequences of transcranial alternating current stimulation. First, we observed that 2 mA currents generated substantial intracranial fields, which were much stronger in the stimulated hemisphere (0.12 V/m) than on the opposite side of the brain (0.03 V/m). Second, we found that brief application of transcranial alternating current stimulation at 10 Hz reduced spike-frequency adaptation of MT neurons and led to a broadband increase in the power spectrum of local field potentials. Together, these findings provide a direct demonstration that weak electric fields applied to the scalp significantly affect neural processing in the primate brain and that this includes a hitherto unknown mechanism that attenuates sensory adaptation. |
Steffen Klingenhoefer; Bart Krekelberg Perisaccadic visual perception Journal Article In: Journal of Vision, vol. 17, no. 9, pp. 1–14, 2017. @article{Klingenhoefer2017,Primates use frequent, rapid eye movements to sample their visual environment. This is a fruitful strategy to make the best use of the highly sensitive foveal part of the retina, but it requires neural mechanisms to bind the rapidly changing visual input into a single, stable percept. Studies investigating these neural mechanisms have typically assumed that perisaccadic perception in nonhuman primates matches that of humans. We tested this assumption by performing identical experiments in human and nonhuman primates. Our data confirm that perisaccadic visual perception of macaques and humans is qualitatively similar. Specifically, we found a reduction in detectability and mislocalization of targets presented at the time of saccades. We also found substantial differences between human and nonhuman primates. Notably, in nonhuman primates, localization that requires knowledge of eye position was less precise, nonhuman primates detected fewer perisaccadic stimuli, and perisaccadic compression was not towards the saccade target. The qualitative similarities between species support the view that the nonhuman primate is ideally suited to study aspects of brain function-such as those relying on foveal vision-that are uniquely developed in primates. The quantitative differences, however, demonstrate the need for a reassessment of the models purportedly linking neural response changes at the time of saccades with the behavioral phenomena of perisaccadic reduction of detectability and mislocalization. |
Matthew R. Krause; Theodoros P. Zanos; Bennett A. Csorba; Praveen K. Pilly; Jaehoon Choe; Matthew E. Phillips; Abhishek Datta; Christopher C. Pack Transcranial direct current stimulation facilitates associative learning and alters functional connectivity in the primate brain Journal Article In: Current Biology, vol. 27, no. 20, pp. 3086–3096, 2017. @article{Krause2017,There has been growing interest in transcranial direct current stimulation (tDCS), a non-invasive technique purported to modulate neural activity via weak, externally applied electric fields. Although some promising preliminary data have been reported for applications ranging from stroke rehabilitation to cognitive enhancement, little is known about how tDCS affects the human brain, and some studies have concluded that it may have no effect at all. Here, we describe a macaque model of tDCS that allows us to simultaneously examine the effects of tDCS on brain activity and behavior. We find that applying tDCS to right prefrontal cortex improves monkeys' performance on an associative learning task. While firing rates do not change within the targeted area, tDCS does induce large low-frequency oscillations in the underlying tissue. These oscillations alter functional connectivity, both locally and between distant brain areas, and these long-range changes correlate with tDCS's effects on behavior. Together, these results are consistent with the idea that tDCS leads to widespread changes in brain activity and suggest that it may be a valuable method for cheaply and non-invasively altering functional connectivity in humans. Krause et al. test transcranial direct current stimulation (tDCS) in a realistic non-human primate model. Stimulation of prefrontal cortex (PFC) improved animals' associative learning while altering coherence between PFC and sensory areas. Their data suggest that tDCS may act by altering long-range connectivity between PFC and other brain areas. |
Matthew L. Leavitt; Florian Pieper; Adam J. Sachs; Julio C. Martinez-Trujillo Correlated variability modifies working memory fidelity in primate prefrontal neuronal ensembles Journal Article In: Proceedings of the National Academy of Sciences, vol. 114, no. 12, pp. E2494–E2503, 2017. @article{Leavitt2017a,Neurons in the primate lateral prefrontal cortex (LPFC) encode working memory (WM) representations via sustained firing, a phenomenon hypothesized to arise from recurrent dynamics within ensembles of interconnected neurons. Here, we tested this hypothesis by using microelectrode arrays to examine spike count correlations (rsc) in LPFC neuronal ensembles during a spatial WM task. We found a pattern of pairwise rsc during WM maintenance indicative of stronger coupling between similarly tuned neurons and increased inhibition between dissimilarly tuned neurons. We then used a linear decoder to quantify the effects of the high-dimensional rsc structure on information coding in the neuronal ensembles. We found that the rsc structure could facilitate or impair coding, depending on the size of the ensemble and tuning properties of its constituent neurons. A simple optimization procedure demonstrated that near-maximum decoding performance could be achieved using a relatively small number of neurons. These WM- optimized subensembles were more signal correlation (rsignal)- diverse and anatomically dispersed than predicted by the statistics of the full recorded population of neurons, and they often con- tained neurons that were poorly WM-selective, yet enhanced cod- ing fidelity by shaping the ensemble's rsc structure. We observed a pattern of rsc between LPFC neurons indicative of recurrent dynamics as a mechanism for WM-related activity and that the rsc structure can increase the fidelity ofWM representations. Thus, WM coding in LPFC neuronal ensembles arises from a complex synergy between single neuron coding properties and multidimensional, ensemble-level phenomena. |
Jeyeon Lee; Hoseok Choi; Seho Lee; Baek Hwan Cho; Kyoung-ha Ahn; In Young Kim; Kyoung-Min Lee; Dong-Pyo Jang Decoding saccadic directions using epidural ECoG in non-human primates Journal Article In: Journal of Korean Medical Science, vol. 32, no. 8, pp. 1243–1250, 2017. @article{Lee2017,A brain-computer interface (BCI) can be used to restore some communication as an alternative interface for patients suffering from locked-in syndrome. However, most BCI systems are based on SSVEP, P300, or motor imagery, and a diversity of BCI protocols would be needed for various types of patients. In this paper, we trained the choice saccade (CS) task in 2 non-human primate monkeys and recorded the brain signal using an epidural electrocorticogram (eECoG) to predict eye movement direction. We successfully predicted the direction of the upcoming eye movement using a support vector machine (SVM) with the brain signals after the directional cue onset and before the saccade execution. The mean accuracies were 80% for 2 directions and 43% for 4 directions. We also quantified the spatial-spectro-temporal contribution ratio using SVM recursive feature elimination (RFE). The channels over the frontal eye field (FEF), supplementary eye field (SEF), and superior parietal lobule (SPL) area were dominantly used for classification. The α-band in the spectral domain and the time bins just after the directional cue onset and just before the saccadic execution were mainly useful for prediction. A saccade based BCI paradigm can be projected in the 2D space, and will hopefully provide an intuitive and convenient communication platform for users. |
Roman F. Loonis; Scott L. Brincat; Evan G. Antzoulatos; Earl K. Miller A meta-analysis suggests different neural correlates for implicit and explicit learning Journal Article In: Neuron, vol. 96, no. 2, pp. 521–534.e7, 2017. @article{Loonis2017,A meta-analysis of non-human primates performing three different tasks (Object-Match, Category-Match, and Category-Saccade associations) revealed signatures of explicit and implicit learning. Performance improved equally following correct and error trials in the Match (explicit) tasks, but it improved more after correct trials in the Saccade (implicit) task, a signature of explicit versus implicit learning. Likewise, error-related negativity, a marker for error processing, was greater in the Match (explicit) tasks. All tasks showed an increase in alpha/beta (10–30 Hz) synchrony after correct choices. However, only the implicit task showed an increase in theta (3–7 Hz) synchrony after correct choices that decreased with learning. In contrast, in the explicit tasks, alpha/beta synchrony increased with learning and decreased thereafter. Our results suggest that explicit versus implicit learning engages different neural mechanisms that rely on different patterns of oscillatory synchrony. Loonis et al. find that explicit and implicit learning use feedback about correct choices versus errors differently. Implicit learning relies more on theta synchrony (3–7 Hz) while explicit learning relies on alpha/beta synchrony (10–30 Hz). |
Nicolas Y. Masse; Jonathan M. Hodnefield; David J. Freedman Mnemonic encoding and cortical organization in parietal and prefrontal cortices Journal Article In: Journal of Neuroscience, vol. 37, no. 25, pp. 6098–6112, 2017. @article{Masse2017,Persistent activity within the frontoparietal network is consistently observed during tasks that require working memory. However, the neural circuit mechanisms underlying persistent neuronal encoding within this network remain unresolved. Here, we ask how neural circuits support persistent activity by examining population recordings from posterior parietal (PPC) and prefrontal (PFC) cortices in two male monkeys that performed spatial and motion direction-based tasks that required working memory. While spatially selective persistent activity was observed in both areas, robust selective persistent activity for motion direction was only observed in PFC. Crucially, we find that this difference between mnemonic encoding in PPC and PFC is associated with the presence offunctional clustering: PPC and PFC neurons up to ~700 μm apart preferred similar spatial locations, and PFC neurons up to ~700 μm apart preferred similar motion directions. In contrast, motion-direction tuning similarity between nearby PPC neurons was much weaker and decayed rapidly beyond ~200 μm. We also observed a similar association between persistent activity and functional clustering in trained recurrent neural network models embedded with a columnar topology. These results suggest that functional clustering facilitates mnemonic encoding of sensory information. |
Bram-Ernst Verhoef; John H. R. Maunsell Attention-related changes in correlated neuronal activity arise from normalization mechanisms Journal Article In: Nature Neuroscience, vol. 20, no. 7, pp. 969–977, 2017. @article{Verhoef2017,Attention is believed to enhance perception by altering the activity-level correlations between pairs of neurons. How attention changes neuronal activity correlations is unknown. Using multielectrodes in monkey visual cortex, we measured spike-count correlations when single or multiple stimuli were presented and when stimuli were attended or unattended. When stimuli were unattended, adding a suppressive, nonpreferred stimulus beside a preferred stimulus increased spike-count correlations between pairs of similarly tuned neurons but decreased spike-count correlations between pairs of oppositely tuned neurons. A stochastic normalization model containing populations of oppositely tuned, mutually suppressive neurons explains these changes and also explains why attention decreased or increased correlations: as an indirect consequence of attention-related changes in the inputs to normalization mechanisms. Our findings link normalization mechanisms to correlated neuronal activity and attention, showing that normalization mechanisms shape response correlations and that these correlations change when attention biases normalization mechanisms. |
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. |
Olga Dal Monte; Matthew Piva; Kevin M. Anderson; Marios Tringides; Avram J. Holmes; Steve W. C. Chang Oxytocin under opioid antagonism leads to supralinear enhancement of social attention Journal Article In: Proceedings of the National Academy of Sciences, vol. 114, no. 20, pp. 5247–5252, 2017. @article{DalMonte2017,To provide new preclinical evidence toward improving the efficacy of oxytocin (OT) in treating social dysfunction, we tested the benefit of administering OT under simultaneously induced opioid antagonism during dyadic gaze interactions in monkeys. OT coadministered with a μ-opioid receptor antagonist, naloxone, invoked a supralinear enhancement of prolonged and selective social attention, producing a stronger effect than the summed effects of each administered separately. These effects were consistently observed when averaging over entire sessions, as well as specifically following events of particular social importance, including mutual eye contact and mutual reward receipt. Furthermore, attention to various facial regions was differentially modulated depending on social context. Using the Allen Institute's transcriptional atlas, we further established the colocalization of μ-opioid and κ-opioid receptor genes and OT genes at the OT-releasing sites in the human brain. These data across monkeys and humans support a regulatory relationship between the OT and opioid systems and suggest that administering OT under opioid antagonism may boost the therapeutic efficacy of OT for enhancing social cognition. |
Nicholas K. DeWind; Jiyun Peng; Andrew Luo; Elizabeth M. Brannon; Michael L. Platt Pharmacological inactivation does not support a unique causal role for intraparietal sulcus in the discrimination of visual number Journal Article In: PLoS ONE, vol. 12, no. 12, pp. e0188820, 2017. @article{DeWind2017,The "number sense" describes the intuitive ability to quantify without counting. Single neu-ron recordings in non-human primates and functional imaging in humans suggest the intra-parietal sulcus is an important neuroanatomical locus of numerical estimation. Other lines of inquiry implicate the IPS in numerous other functions, including attention and decision mak-ing. Here we provide a direct test of whether IPS has functional specificity for numerosity judgments. We used muscimol to reversibly and independently inactivate the ventral and lat-eral intraparietal areas in two monkeys performing a numerical discrimination task and a color discrimination task, roughly equilibrated for difficulty. Inactivation of either area caused parallel impairments in both tasks and no evidence of a selective deficit in numerical pro-cessing. These findings do not support a causal role for the IPS in numerical discrimination, except insofar as it also has a role in the discrimination of color. We discuss our findings in light of several alternative hypotheses of IPS function, including a role in orienting responses, a general cognitive role in attention and decision making processes and a more specific role in ordinal comparison that encompasses both number and color judgments. |
Kacie Dougherty; Michele A. Cox; Taihei Ninomiya; David A. Leopold; Alexander Maier Ongoing alpha activity in V1 regulates visually driven spiking responses Journal Article In: Cerebral Cortex, vol. 27, no. 2, pp. 1113–1124, 2017. @article{Dougherty2017,The interlaminar connections in the primate primary visual cortex (V1) are well described, as is the presence of ongoing alpha-range (7-14 Hz) fluctuations in this area. Less well understood is how these interlaminar connections and ongoing fluctuations contribute to the regulation of visual spiking responses. Here, we investigate the relationship between alpha fluctuations and spiking responses to visual stimuli across cortical layers. Using laminar probes in macaque V1, we show that neural firing couples with the phase of alpha fluctuations, and that magnitude of this coupling is particularly pronounced during visual stimulation. The strongest modulation of spiking activity was observed in layers 2/3. Alpha-spike coupling and current source density analysis pointed to an infragranular origin of the alpha fluctuations. Taken together, these results indicate that ongoing infragranular alpha-range fluctuations in V1 play a role in regulating columnar visual activity. |
R. Becket Ebitz; Tirin Moore Selective modulation of the pupil light reflex by microstimulation of prefrontal cortex Journal Article In: Journal of Neuroscience, vol. 37, no. 19, pp. 5008–5018, 2017. @article{Ebitz2017,The prefrontal cortex (PFC) is thought to flexibly regulate sensorimotor responses, perhaps through modulating activity in other circuits. However, the scope of that control remains unknown: it remains unclear whether the PFC can modulate basic reflexes. One canonical example of a central reflex is the pupil light reflex (PLR): the automatic constriction of the pupil in response to luminance increments. Unlike pupil size, which depends on the interaction of multiple physiological and neuromodulatory influences, the PLR reflects the action of a simple brainstem circuit. However, emerging behavioral evidence suggests that the PLR may be modulated by cognitive processes. Although the neural basis of these modulations remains unknown, one possible source is the PFC, particularly the frontal eye field (FEF), an area of the PFC implicated in the control of attention. We show that microstimulation of the rhesus macaque FEF alters the magnitude of the PLR in a spatially specific manner. FEF microstimulation enhanced the PLR to probes presented within the stimulated visual field, but suppressed the PLR to probes at nonoverlapping locations. The spatial specificity of this effect parallels the effect of FEF stimulation on attention and suggests that FEF is capable of modulating visuomotor transformations performed at a lower level than was previously known. These results provide evidence of the selective regulation of a basic brainstem reflex by the PFC. |
Hongwei Fan; Xiaochuan Pan; Rubin Wang; Masamichi Sakagami Differences in reward processing between putative cell types in primate prefrontal cortex Journal Article In: PLoS ONE, vol. 12, no. 12, pp. e0189771, 2017. @article{Fan2017a,Single-unit studies in monkeys have demonstrated that neurons in the prefrontal cortex predict the reward type, reward amount or reward availability associated with a stimulus. To examine contributions of pyramidal cells and interneurons in reward processing, single-unit activity was extracellularly recorded in prefrontal cortices of four monkeys performing a reward prediction task. Based on their shapes of spike waveforms, prefrontal neurons were classified into broad-spike and narrow-spike units that represented putative pyramidal cells and interneurons, respectively. We mainly observed that narrow-spike neurons showed higher firing rates but less bursty discharges than did broad-spike neurons. Both narrow-spike and broad-spike cells selectively responded to the stimulus, reward and their interaction, and the proportions of each type of selective neurons were similar between the two cell classes. Moreover, the two types of cells displayed equal reliability of reward or stimulus discrimination. Furthermore, we found that broad-spike and narrow-spike cells showed distinct mechanisms for encoding reward or stimulus information. Broad-spike neurons raised their firing rate relative to the baseline rate to represent the preferred reward or stimulus information, whereas narrow-spike neurons inhibited their firing rate lower than the baseline rate to encode the non-preferred reward or stimulus information. Our results suggest that narrow-spike and broad-spike cells were equally involved in reward and stimulus processing in the prefrontal cortex. They utilized a binary strategy to complementarily represent reward or stimulus information, which was consistent with the task structure in which the monkeys were required to remember two reward conditions and two visual stimuli. |
Amber M. Fyall; Yasmine El-Shamayleh; Hannah Choi; Eric Shea-Brown; Anitha Pasupathy Dynamic representation of partially occluded objects in primate prefrontal and visual cortex Journal Article In: eLife, vol. 6, pp. 1–25, 2017. @article{Fyall2017,Successful recognition of partially occluded objects is presumed to involve dynamic interactions between brain areas responsible for vision and cognition, but neurophysiological evidence for the involvement of feedback signals is lacking. Here, we demonstrate that neurons in the ventrolateral prefrontal cortex (vlPFC) of monkeys performing a shape discrimination task respond more strongly to occluded than unoccluded stimuli. In contrast, neurons in visual area V4 respond more strongly to unoccluded stimuli. Analyses of V4 response dynamics reveal that many neurons exhibit two transient response peaks, the second of which emerges after vlPFC response onset and displays stronger selectivity for occluded shapes. We replicate these findings using a model of V4/vlPFC interactions in which occlusion-sensitive vlPFC neurons feed back to shape- selective V4 neurons, thereby enhancing V4 responses and selectivity to occluded shapes. These results reveal how signals from frontal and visual cortex could interact to facilitate object recognition under occlusion. |
Diego A. Gutnisky; Charles B. Beaman; Sergio E. Lew; Valentin Dragoi Spontaneous fluctuations in visual cortical responses influence population coding accuracy Journal Article In: Cerebral Cortex, vol. 27, no. 2, pp. 1409–1427, 2017. @article{Gutnisky2017,Information processing in the cerebral cortex depends not only on the nature of incoming stimuli, but also on the state of neuronal networks at the time of stimulation. That is, the same stimulus will be processed differently depending on the neuronal context in which it is received. A major factor that could influence neuronal context is the background, or ongoing neuronal activity before stimulation. In visual cortex, ongoing activity is known to play a critical role in the development of local circuits, yet whether it influences the coding of visual features in adult cortex is unclear. Here, we investigate whether and how the information encoded by individual neurons and populations in primary visual cortex (V1) depends on the ongoing activity before stimulus presentation. We report that when individual neurons are in a "low" prestimulus state, they have a higher capacity to discriminate stimulus features, such as orientation, despite their reduction in evoked responses. By measuring the distribution of prestimulus activity across a population of neurons, we found that network discrimination accuracy is improved in the low prestimulus state. Thus, the distribution of ongoing activity states across the network creates an "internal context" that dynamically filters incoming stimuli to modulate the accuracy of sensory coding. The modulation of stimulus coding by ongoing activity state is consistent with recurrent network models in which ongoing activity dynamically controls the balanced background excitation and inhibition to individual neurons. |
Diego A. Gutnisky; Charles Beaman; Sergio E. Lew; Valentin Dragoi Cortical response states for enhanced sensory discrimination Journal Article In: eLife, vol. 6, pp. 1–23, 2017. @article{Gutnisky2017a,Brain activity during wakefulness is characterized by rapid fluctuations in neuronal responses. Whether these fluctuations play any role in modulating the accuracy of behavioral responses is poorly understood. Here, we investigated whether and how trial changes in the population response impact sensory coding in monkey V1 and perceptual performance. Although the responses of individual neurons varied widely across trials, many cells tended to covary with the local population. When population activity was in a 'low' state, neurons had lower evoked responses and correlated variability, yet higher probability to predict perceptual accuracy. The impact of firing rate fluctuations on network and perceptual accuracy was strongest 200-ms before stimulus presentation, and it greatly diminished when the number of cells used to measure the state of the population was decreased. These findings indicate that enhanced perceptual discrimination occurs when population activity is in a 'silent' response mode in which neurons increase information extraction. |
Gerald Hahn; Adrian Ponce-Alvarez; Cyril Monier; Giacomo Benvenuti; Arvind Kumar; Frédéric Chavane; Gustavo Deco; Yves Frégnac Spontaneous cortical activity is transiently poised close to criticality Journal Article In: PLoS Computational Biology, vol. 13, no. 5, pp. e1005543, 2017. @article{Hahn2017,Brain activity displays a large repertoire of dynamics across the sleep-wake cycle and even during anesthesia. It was suggested that criticality could serve as a unifying principle underlying the diversity of dynamics. This view has been supported by the observation of spontaneous bursts of cortical activity with scale-invariant sizes and durations, known as neuronal avalanches, in recordings of mesoscopic cortical signals. However, the existence of neuronal avalanches in spiking activity has been equivocal with studies reporting both its presence and absence. Here, we show that signs of criticality in spiking activity can change between synchronized and desynchronized cortical states. We analyzed the spontaneous activity in the primary visual cortex of the anesthetized cat and the awake monkey, and found that neuronal avalanches and thermodynamic indicators of criticality strongly depend on collective synchrony among neurons, LFP fluctuations, and behavioral state. We found that synchronized states are associated to criticality, large dynamical repertoire and prolonged epochs of eye closure, while desynchronized states are associated to sub-criticality, reduced dynamical repertoire, and eyes open conditions. Our results show that criticality in cortical dynamics is not stationary, but fluctuates during anesthesia and between different vigilance states. |
S. A. Hassani; Mariann Oemisch; M. Balcarras; Stephanie Westendorff; S. Ardid; M. A. Meer; P. Tiesinga; T. Womelsdorf In: Scientific Reports, vol. 7, pp. 40606, 2017. @article{Hassani2017,Noradrenaline is believed to support cognitive flexibility through the alpha 2A noradrenergic receptor (a2A-NAR) acting in prefrontal cortex. Enhanced flexibility has been inferred from improved working memory with the a2A-NA agonist Guanfacine. But it has been unclear whether Guanfacine improves specific attention and learning mechanisms beyond working memory, and whether the drug effects can be formalized computationally to allow single subject predictions. We tested and confirmed these suggestions in a case study with a healthy nonhuman primate performing a feature-based reversal learning task evaluating performance using Bayesian and Reinforcement learning models. In an initial dose-testing phase we found a Guanfacine dose that increased performance accuracy, decreased distractibility and improved learning. In a second experimental phase using only that dose we examined the faster feature-based reversal learning with Guanfacine with single-subject computational modeling. Parameter estimation suggested that improved learning is not accounted for by varying a single reinforcement learning mechanism, but by changing the set of parameter values to higher learning rates and stronger suppression of non-chosen over chosen feature information. These findings provide an important starting point for developing nonhuman primate models to discern the synaptic mechanisms of attention and learning functions within the context of a computational neuropsychiatry framework. |
James P. Herman; Richard J. Krauzlis Color-change detection activity in the primate superior colliculus Journal Article In: eNeuro, vol. 4, no. 2, pp. 1–16, 2017. @article{Herman2017,The primate superior colliculus (SC) is a midbrain structure that participates in the control of spatial attention. Previous studies examining the role of the SC in attention have mostly used luminance-based visual features (e.g., motion, contrast) as the stimuli and saccadic eye movements as the behavioral response, both of which are known to modulate the activity of SC neurons. To explore the limits of the SC's involvement in the control of spatial attention, we recorded SC neuronal activity during a task using color, a visual feature dimension not traditionally associated with the SC, and required monkeys to detect threshold-level changes in the saturation of a cued stimulus by releasing a joystick during maintained fixation. Using this color-based spatial attention task, we found substantial cue-related modulation in all categories of visually responsive neurons in the intermediate layers of the SC. Notably, near-threshold changes in color saturation, both increases and decreases, evoked phasic bursts of activity with magnitudes as large as those evoked by stimulus onset. This change-detection activity had two distinctive features: activity for hits was larger than for misses, and the timing of change-detection activity accounted for 67% of joystick release latency, even though it preceded the release by at least 200 ms. We conclude that during attention tasks, SC activity denotes the behavioral relevance of the stimulus regardless of feature dimension and that phasic event-related SC activity is suitable to guide the selection of manual responses as well as saccadic eye movements. |
Markus A. Hietanen; Nicholas S. C. Price; Shaun L. Cloherty; Kostas Hadjidimitrakis; Michael R. Ibbotson Long-term sensorimotor adaptation in the ocular following system of primates Journal Article In: PLoS ONE, vol. 12, no. 12, pp. e0189030, 2017. @article{Hietanen2017,The sudden movement of a wide-field image leads to a reflexive eye tracking response referred to as short-latency ocular following. If the image motion occurs soon after a saccade the initial speed of the ocular following is enhanced, a phenomenon known as post-saccadic enhancement. We show in macaque monkeys that repeated exposure to the same stimulus regime over a period of months leads to progressive increases in the initial speeds of ocular following. The improvement in tracking speed occurs for ocular following with and without a prior saccade. As a result of the improvement in ocular following speeds, the influence of post-saccadic enhancement wanes with increasing levels of training. The improvement in ocular following speed following repeated exposure to the same oculomotor task represents a novel form of sensori-motor learning in the context of a reflexive movement. |
Guilhem Ibos; David J. Freedman Sequential sensory and decision processing in posterior parietal cortex Journal Article In: eLife, vol. 6, pp. 1–19, 2017. @article{Ibos2017,<p>Decisions about the behavioral significance of sensory stimuli often require comparing sensory inference of what we are looking at to internal models of what we are looking for. Here, we test how neuronal selectivity for visual features is transformed into decision-related signals in posterior parietal cortex (area LIP). Monkeys performed a visual matching task that required them to detect target stimuli composed of conjunctions of color and motion-direction. Neuronal recordings from area LIP revealed two main findings. First, the sequential processing of visual features and the selection of target-stimuli suggest that LIP is involved in transforming sensory information into decision-related signals. Second, the patterns of color and motion selectivity and their impact on decision-related encoding suggest that LIP plays a role in detecting target stimuli by comparing bottom-up sensory inputs (what the monkeys were looking at) and top-down cognitive encoding inputs (what the monkeys were looking for).</p> |
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{So2016,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. |
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{Romero2016,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{Ruff2016b,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{Ruff2016a,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{Sarma2016,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{Skoblenick2016,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{Sleezer2016a,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{Snyder2016,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. |
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). |
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. |
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. |
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. |