Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex

1. Single-neuron activity was recorded from the prefrontal cortex of monkeys performing saccadic eye movements in oculomotor delayed-response (ODR) and visually guided saccade (VGS) tasks. In the ODR task the monkey was required to maintain fixation of a central spot throughout the 0.5-s cue and 3.0-s delay before making a saccadic eye movement in the dark to one of four or eight locations where the visual cue had been presented. The same locations were used for targets in the VGS tasks; however, unlike the ODR task, saccades in the VGS tasks were visually guided. 2. Among 434 neurons recorded from prefrontal cortex within and surrounding the principal sulcus (PS), 147 changed their discharge rates in relation to saccadic eye movements in the ODR task. Their response latencies relative to saccade initiation were distributed between -192 and 460-ms, with 22% exhibiting presaccadic activity and 78% exhibiting only postsaccadic activity. Among PS neurons with presaccadic activity, 53% also had postsaccadic activity when the monkey made saccadic eye movements opposite to the directions for which the presaccadic activity was observed. 3. Almost all (97%) PS neurons with presaccadic activity were directionally selective. The best direction and tuning specificity of each neuron were estimated from parameters used to fit a Gaussian tuning curve function. The best direction for 62% of the neurons with presaccadic activity was toward the contralateral visual field, with the remaining neurons having best directions toward the ipsilateral field (23%) or along the vertical meridian (15%). 4. Most postsaccadic activity of PS neurons (92%) was also directionally selective. The best direction for 48% of these neurons was toward the contralateral visual field, with the remaining neurons having best directions toward the ipsilateral field (36%) or along the vertical meridian (16%). Eighteen percent of the neurons with postsaccadic activity showed a reciprocal response pattern: excitatory responses occurred for one set of saccade directions, whereas inhibitory responses occurred for roughly the opposite set of directions. 5. Sixty PS neurons with saccade-related activity in the ODR task were also examined in a VGS task. Forty of these neurons showed highly similar profiles of directional specificity and response magnitude in both tasks, 13 showed saccade-related activity only in the ODR task, and 7 changed their response characteristics between the ODR and VGS tasks.(ABSTRACT TRUNCATED AT 400 WORDS)

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Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms

Journal of Neurophysiology ◽

10.1152/jn.1990.63.4.814 ◽

1990 ◽

Vol 63 (4) ◽

pp. 814-831 ◽

Cited By ~ 255

Author(s):

S. Funahashi ◽

C. J. Bruce ◽

P. S. Goldman-Rakic

Keyword(s):

Prefrontal Cortex ◽

Visual Field ◽

Visual Cues ◽

Neuron Activity ◽

Delayed Response ◽

Visual Response ◽

Visual Responses ◽

Directional Tuning ◽

Vertical Meridian ◽

Visual Probe

1. Visual responses and their relationship to delay-period activity were studied by recording single neuron activity from the prefrontal cortex of rhesus monkeys while they performed an oculomotor delayed-response (ODR) and a visual probe (VP) task. In the ODR task, the monkey was required to maintain fixation of a central spot of light throughout the cue (0.5 s) and delay (3 s) periods and then make a saccadic eye movement to one of four or eight locations where the visual cue had been presented. In the VP task, the same visual stimuli that were used in the ODR task were presented for 0.5 s, but no response was required. The VP task was thus employed to test the passive visual response and, by comparison with cue-elicited activity in the ODR task, to examine the degree of behavioral enhancement present in prefrontal visual activity. 2. Among 434 neurons recorded from the prefrontal cortex within and surrounding the principal sulcus (PS), 261 had task-related activity during at least one phase of the ODR task, and 74 of these had phasic visual responses to the onset of the visual cues with a median latency of 116 ms. The visual responses of 69 neurons were excitatory, and 5 neurons were inhibited. Five of the neurons with excitatory visual responses also responded transiently after the offset of the cue. 3. Visual responses were classified as directional for 71 PS neurons (96%) in that excitatory or inhibitory responses occurred only for location of cues in a restricted portion of the visual field. Only 3 PS neurons were omnidirectional, i.e., responded equivalently to cues in all locations tested. 4. The best direction and tuning specificity of all PS neurons with directional visual responses were estimated from parameters yielding the best fit to a Gaussian-shaped tuning function. The best direction for the majority (71%) of neurons was toward the visual field contralateral to the hemisphere where the neuron was located. The remaining neurons had their best directions in the ipsilateral field (18%) or along the vertical meridian (11%). 5. The specificity of directional tuning for PS visual responses was quite variable, ranging from neurons that responded only to one of the eight cue locations to neurons that responded to all eight, but in a clearly graded fashion. The standard deviation parameter of the Gaussian curve indexed the breadth of directional tuning of each neuron; its median value was 37 degrees.(ABSTRACT TRUNCATED AT 400 WORDS)

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Prefrontal Task-Related Activity Representing Visual Cue Location or Saccade Direction in Spatial Working Memory Tasks

Journal of Neurophysiology ◽

10.1152/jn.00249.2001 ◽

2002 ◽

Vol 87 (1) ◽

pp. 567-588 ◽

Cited By ~ 105

Author(s):

Kazuyoshi Takeda ◽

Shintaro Funahashi

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Spatial Working Memory ◽

Delay Period ◽

Neuron Activity ◽

Delayed Response ◽

Related Activity ◽

Visual Cue ◽

Response Period ◽

Dorsolateral Prefrontal

To examine what kind of information task-related activity encodes during spatial working memory processes, we analyzed single-neuron activity in the prefrontal cortex while two monkeys performed two different oculomotor delayed-response (ODR) tasks. In the standard ODR task, monkeys were required to make a saccade to the cue location after a 3-s delay, whereas in the rotatory ODR (R-ODR) task, they were required to make a saccade 90° clockwise from the cue location after the 3-s delay. By comparing the same task-related activities in these two tasks, we could determine whether such activities encoded the location of the visual cue or the direction of the saccade. One hundred twenty one neurons exhibited task-related activity in relation to at least one task event in both tasks. Among them, 41 neurons exhibited directional cue-period activity, most of which encoded the location of the visual cue. Among 56 neurons with directional delay-period activity, 86% encoded the location of the visual cue, whereas 13% encoded the direction of the saccade. Among 57 neurons with directional response-period activity, 58% encoded the direction of the saccade, whereas 35% encoded the location of the visual cue. Most neurons whose response-period activity encoded the location of the visual cue also exhibited directional delay-period activity that encoded the location of the visual cue as well. The best directions of these two activities were identical, and most of these response-period activities were postsaccadic. Therefore this postsaccadic activity can be considered a signal to terminate unnecessary delay-period activity. Population histograms encoding the location of the visual cue showed tonic sustained activation during the delay period. However, population histograms encoding the direction of the saccade showed a gradual increase in activation during the delay period. These results indicate that the transformation from visual input to motor output occurs in the dorsolateral prefrontal cortex. The analysis using population histograms suggests that this transformation occurs gradually during the delay period.

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Reversible Inactivation of Monkey Superior Colliculus. I. Curvature of Saccadic Trajectory

Journal of Neurophysiology ◽

10.1152/jn.1998.79.4.2082 ◽

1998 ◽

Vol 79 (4) ◽

pp. 2082-2096 ◽

Cited By ~ 102

Author(s):

Hiroshi Aizawa ◽

Robert H. Wurtz

Keyword(s):

Eye Movements ◽

Visual Field ◽

Superior Colliculus ◽

Saccadic Eye Movements ◽

Cell Types ◽

Neuron Activity ◽

Eye Position ◽

Two Dimensional ◽

Reversible Inactivation ◽

Intermediate Layers

Aizawa, Hiroshi and Robert H. Wurtz. Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. J. Neurophysiol. 79: 2082–2096, 1998. The neurons in the intermediate layers of the monkey superior colliculus (SC) that discharge before saccadic eye movements can be divided into at least two types, burst and buildup neurons, and the differences in their characteristics are compatible with different functional contributions of the two cell types. It has been suggested that a spread of activity across the population of the buildup neurons during saccade generation may contribute to the control of saccadic eye movements. The influence of any such spread should be on both the horizontal and vertical components of the saccade because the map of the movement fields on the SC is a two-dimensional one; it should affect the trajectory of saccade. The present experiments used muscimol injections to inactivate areas within the SC to determine the functional contribution of such a spread of activity on the trajectory of the saccades. The analysis concentrated on saccades made to areas of the visual field that should be affected primarily by alteration of buildup neuron activity. Muscimol injections produced saccades with altered trajectories; they became consistently curved after the injection, and successive saccades to the same targets had similar curvatures. The curved saccades showed changes in their direction and speed at the very beginning of the saccade, and for those saccades that reached the target, the direction of the saccade was altered near the end to compensate for the initially incorrect direction. Postinjection saccades had lower peak speeds, longer durations, and longer latencies for initiation. The changes in saccadic trajectories resulting from muscimol injections, along with the previous observations on changes in speed of saccades with such injections, indicate that the SC is involved in influencing the eye position during the saccade as well as at the end of the saccade. The changes in trajectory when injections were made more rostral in the SC than the most active burst neurons also are consistent with a contribution of the buildup neurons to the control of the eye trajectory. The results do not, however, support the hypothesis that the buildup neurons in the SC act as a spatial integrator.

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Vision as oculomotor reward: cognitive contributions to the dynamic control of saccadic eye movements

Cognitive Neurodynamics ◽

10.1007/s11571-020-09661-y ◽

2021 ◽

Author(s):

Christian Wolf ◽

Markus Lappe

Keyword(s):

Eye Movements ◽

Visual Field ◽

Visual System ◽

Dynamic Control ◽

Saccadic Eye Movements ◽

Saccade Target ◽

Cognitive Mechanisms ◽

Foveal Vision ◽

Subsequent Behavior ◽

High Level

AbstractHumans and other primates are equipped with a foveated visual system. As a consequence, we reorient our fovea to objects and targets in the visual field that are conspicuous or that we consider relevant or worth looking at. These reorientations are achieved by means of saccadic eye movements. Where we saccade to depends on various low-level factors such as a targets’ luminance but also crucially on high-level factors like the expected reward or a targets’ relevance for perception and subsequent behavior. Here, we review recent findings how the control of saccadic eye movements is influenced by higher-level cognitive processes. We first describe the pathways by which cognitive contributions can influence the neural oculomotor circuit. Second, we summarize what saccade parameters reveal about cognitive mechanisms, particularly saccade latencies, saccade kinematics and changes in saccade gain. Finally, we review findings on what renders a saccade target valuable, as reflected in oculomotor behavior. We emphasize that foveal vision of the target after the saccade can constitute an internal reward for the visual system and that this is reflected in oculomotor dynamics that serve to quickly and accurately provide detailed foveal vision of relevant targets in the visual field.

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Effects of unilateral deactivations of dorsolateral prefrontal cortex and anterior cingulate cortex on saccadic eye movements

Journal of Neurophysiology ◽

10.1152/jn.00626.2013 ◽

2014 ◽

Vol 111 (4) ◽

pp. 787-803 ◽

Cited By ~ 12

Author(s):

Michael J. Koval ◽

R. Matthew Hutchison ◽

Stephen G. Lomber ◽

Stefan Everling

Keyword(s):

Prefrontal Cortex ◽

Eye Movements ◽

Functional Connectivity ◽

Anterior Cingulate Cortex ◽

Dorsolateral Prefrontal Cortex ◽

Saccadic Eye Movements ◽

Cingulate Cortex ◽

Anterior Cingulate ◽

Dorsolateral Prefrontal ◽

Single Neuron Recording

The dorsolateral prefrontal cortex (dlPFC) and anterior cingulate cortex (ACC) have both been implicated in the cognitive control of saccadic eye movements by single neuron recording studies in nonhuman primates and functional imaging studies in humans, but their relative roles remain unclear. Here, we reversibly deactivated either dlPFC or ACC subregions in macaque monkeys while the animals performed randomly interleaved pro- and antisaccades. In addition, we explored the whole-brain functional connectivity of these two regions by applying a seed-based resting-state functional MRI analysis in a separate cohort of monkeys. We found that unilateral dlPFC deactivation had stronger behavioral effects on saccades than unilateral ACC deactivation, and that the dlPFC displayed stronger functional connectivity with frontoparietal areas than the ACC. We suggest that the dlPFC plays a more prominent role in the preparation of pro- and antisaccades than the ACC.

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Representation of actions and outcomes in medial prefrontal cortex during delayed conditional decision-making: Population analyses of single neuron activity

Brain and Neuroscience Advances ◽

10.1177/2398212818773865 ◽

2018 ◽

Vol 2 ◽

pp. 239821281877386 ◽

Cited By ~ 2

Author(s):

Miranda J. Francoeur ◽

Robert G. Mair

Keyword(s):

Decision Making ◽

Prefrontal Cortex ◽

Medial Prefrontal Cortex ◽

Single Neuron ◽

Neuron Activity ◽

Related Activity ◽

Response Options ◽

Single Neuron Activity ◽

Temporal Organisation ◽

Matching To Position

Background: To respond adaptively in a dynamic environment, it is important for organisms to utilise information about recent events to decide between response options. Methods: To examine the role of medial prefrontal cortex in adaptive decision-making, we recorded single neuron activity in rats performing a dynamic delayed non-matching to position task. Results: We recorded activity from 1335 isolated neurons, 458 (34%) with criterion event-related activity, of which 431 (94%) exhibited 1 of 10 distinct excitatory response types: five at different times relative to delivery (or lack) of reinforcement following sample and choice responses and five correlated with movements or lever press actions that occurred multiple times in each trial. Normalised population averages revealed a precisely timed cascade of population responses representing the temporal organisation behavioural events that constitute delayed non-matching to position trials. Firing field analyses identified a subset of neurons with restricted spatial fields: responding to the conjunction of a behavioural event with a specific location. Anatomical analyses showed considerable overlap in the distribution of different response types in medial prefrontal cortex with a significant trend for dorsal areas to contain more neurons with action-related activity and ventral areas more responses related to action outcomes. Conclusion: These results indicate that medial prefrontal cortex contains discrete populations of neurons that represent the temporal organisation of actions and outcomes during delayed non-matching to position trials. They support the hypothesis that medial prefrontal cortex promotes flexible control of complex behaviours by action–outcome contingencies.

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Quick phases control ocular torsion during smooth pursuit

Journal of Neurophysiology ◽

10.1152/jn.00194.2011 ◽

2011 ◽

Vol 106 (5) ◽

pp. 2151-2166 ◽

Cited By ~ 2

Author(s):

Bernhard J. M. Hess ◽

Jakob S. Thomassen

Keyword(s):

Eye Movements ◽

Visual Field ◽

Rotation Axis ◽

Three Dimensional ◽

Oculomotor Control ◽

Visually Guided ◽

Open Questions ◽

Spatial Frequencies ◽

Eye Rotation ◽

Smooth Tracking

One of the open questions in oculomotor control of visually guided eye movements is whether it is possible to smoothly track a target along a curvilinear path across the visual field without changing the torsional stance of the eye. We show in an experimental study of three-dimensional eye movements in subhuman primates ( Macaca mulatta) that although the pursuit system is able to smoothly change the orbital orientation of the eye's rotation axis, the smooth ocular motion was interrupted every few hundred milliseconds by a small quick phase with amplitude <1.5° while the animal tracked a target along a circle or ellipse. Specifically, during circular pursuit of targets moving at different angular eccentricities (5°, 10°, and 15°) relative to straight ahead at spatial frequencies of 0.067 and 0.1 Hz, the torsional amplitude of the intervening quick phases was typically around 1° or smaller and changed direction for clockwise vs. counterclockwise tracking. Reverse computations of the eye rotation based on the recorded angular eye velocity showed that the quick phases facilitate the overall control of ocular orientation in the roll plane, thereby minimizing torsional disturbances of the visual field. On the basis of a detailed kinematic analysis, we suggest that quick phases during curvilinear smooth tracking serve to minimize deviations from Donders' law, which are inevitable due to the spherical configuration space of smooth eye movements.

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Stable population coding for working memory coexists with heterogeneous neural dynamics in prefrontal cortex

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1619449114 ◽

2016 ◽

Vol 114 (2) ◽

pp. 394-399 ◽

Cited By ~ 128

Author(s):

John D. Murray ◽

Alberto Bernacchia ◽

Nicholas A. Roy ◽

Christos Constantinidis ◽

Ranulfo Romo ◽

...

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Neural Circuit ◽

Temporal Dynamics ◽

Population Level ◽

Population Coding ◽

Neural Dynamics ◽

Stable Population ◽

Neuron Activity ◽

Delayed Response

Working memory (WM) is a cognitive function for temporary maintenance and manipulation of information, which requires conversion of stimulus-driven signals into internal representations that are maintained across seconds-long mnemonic delays. Within primate prefrontal cortex (PFC), a critical node of the brain’s WM network, neurons show stimulus-selective persistent activity during WM, but many of them exhibit strong temporal dynamics and heterogeneity, raising the questions of whether, and how, neuronal populations in PFC maintain stable mnemonic representations of stimuli during WM. Here we show that despite complex and heterogeneous temporal dynamics in single-neuron activity, PFC activity is endowed with a population-level coding of the mnemonic stimulus that is stable and robust throughout WM maintenance. We applied population-level analyses to hundreds of recorded single neurons from lateral PFC of monkeys performing two seminal tasks that demand parametric WM: oculomotor delayed response and vibrotactile delayed discrimination. We found that the high-dimensional state space of PFC population activity contains a low-dimensional subspace in which stimulus representations are stable across time during the cue and delay epochs, enabling robust and generalizable decoding compared with time-optimized subspaces. To explore potential mechanisms, we applied these same population-level analyses to theoretical neural circuit models of WM activity. Three previously proposed models failed to capture the key population-level features observed empirically. We propose network connectivity properties, implemented in a linear network model, which can underlie these features. This work uncovers stable population-level WM representations in PFC, despite strong temporal neural dynamics, thereby providing insights into neural circuit mechanisms supporting WM.

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