scholarly journals Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms

1990 ◽  
Vol 63 (4) ◽  
pp. 814-831 ◽  
Author(s):  
S. Funahashi ◽  
C. J. Bruce ◽  
P. S. Goldman-Rakic

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)

1991 ◽  
Vol 65 (6) ◽  
pp. 1464-1483 ◽  
Author(s):  
S. Funahashi ◽  
C. J. Bruce ◽  
P. S. Goldman-Rakic

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)


1989 ◽  
Vol 61 (2) ◽  
pp. 331-349 ◽  
Author(s):  
S. Funahashi ◽  
C. J. Bruce ◽  
P. S. Goldman-Rakic

1. An oculomotor delayed-response task was used to examine the spatial memory functions of neurons in primate prefrontal cortex. Monkeys were trained to fixate a central spot during a brief presentation (0.5 s) of a peripheral cue and throughout a subsequent delay period (1-6 s), and then, upon the extinction of the fixation target, to make a saccadic eye movement to where the cue had been presented. Cues were usually presented in one of eight different locations separated by 45 degrees. This task thus requires monkeys to direct their gaze to the location of a remembered visual cue, controls the retinal coordinates of the visual cues, controls the monkey's oculomotor behavior during the delay period, and also allows precise measurement of the timing and direction of the relevant behavioral responses. 2. Recordings were obtained from 288 neurons in the prefrontal cortex within and surrounding the principal sulcus (PS) while monkeys performed this task. An additional 31 neurons in the frontal eye fields (FEF) region within and near the anterior bank of the arcuate sulcus were also studied. 3. Of the 288 PS neurons, 170 exhibited task-related activity during at least one phase of this task and, of these, 87 showed significant excitation or inhibition of activity during the delay period relative to activity during the intertrial interval. 4. Delay period activity was classified as directional for 79% of these 87 neurons in that significant responses only occurred following cues located over a certain range of visual field directions and were weak or absent for other cue directions. The remaining 21% were omnidirectional, i.e., showed comparable delay period activity for all visual field locations tested. Directional preferences, or lack thereof, were maintained across different delay intervals (1-6 s). 5. For 50 of the 87 PS neurons, activity during the delay period was significantly elevated above the neuron's spontaneous rate for at least one cue location; for the remaining 37 neurons only inhibitory delay period activity was seen. Nearly all (92%) neurons with excitatory delay period activity were directional and few (8%) were omnidirectional. Most (62%) neurons with purely inhibitory delay period activity were directional, but a substantial minority (38%) was omnidirectional. 6. Fifteen of the neurons with excitatory directional delay period activity also had significant inhibitory delay period activity for other cue directions. These inhibitory responses were usually strongest for, or centered about, cue directions roughly opposite those optimal for excitatory responses.(ABSTRACT TRUNCATED AT 400 WORDS)


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Stefano Rozzi ◽  
Marco Bimbi ◽  
Alfonso Gravante ◽  
Luciano Simone ◽  
Leonardo Fogassi

AbstractThe ventral part of lateral prefrontal cortex (VLPF) of the monkey receives strong visual input, mainly from inferotemporal cortex. It has been shown that VLPF neurons can show visual responses during paradigms requiring to associate arbitrary visual cues to behavioral reactions. Further studies showed that there are also VLPF neurons responding to the presentation of specific visual stimuli, such as objects and faces. However, it is largely unknown whether VLPF neurons respond and differentiate between stimuli belonging to different categories, also in absence of a specific requirement to actively categorize or to exploit these stimuli for choosing a given behavior. The first aim of the present study is to evaluate and map the responses of neurons of a large sector of VLPF to a wide set of visual stimuli when monkeys simply observe them. Recent studies showed that visual responses to objects are also present in VLPF neurons coding action execution, when they are the target of the action. Thus, the second aim of the present study is to compare the visual responses of VLPF neurons when the same objects are simply observed or when they become the target of a grasping action. Our results indicate that: (1) part of VLPF visually responsive neurons respond specifically to one stimulus or to a small set of stimuli, but there is no indication of a “passive” categorical coding; (2) VLPF neuronal visual responses to objects are often modulated by the task conditions in which the object is observed, with the strongest response when the object is target of an action. These data indicate that VLPF performs an early passive description of several types of visual stimuli, that can then be used for organizing and planning behavior. This could explain the modulation of visual response both in associative learning and in natural behavior.


2016 ◽  
Vol 114 (2) ◽  
pp. 394-399 ◽  
Author(s):  
John D. Murray ◽  
Alberto Bernacchia ◽  
Nicholas A. Roy ◽  
Christos Constantinidis ◽  
Ranulfo Romo ◽  
...  

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.


2002 ◽  
Vol 87 (1) ◽  
pp. 567-588 ◽  
Author(s):  
Kazuyoshi Takeda ◽  
Shintaro Funahashi

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.


2005 ◽  
Vol 94 (4) ◽  
pp. 2491-2503 ◽  
Author(s):  
Keith A. Schneider ◽  
Sabine Kastner

The superior colliculus (SC) is a multimodal laminar structure located on the roof of the brain stem. The SC is a key structure in a distributed network of areas that mediate saccadic eye movements and shifts of attention across the visual field and has been extensively studied in nonhuman primates. In humans, it has proven difficult to study the SC with functional MRI (fMRI) because of its small size, deep location, and proximity to pulsating vascular structures. Here, we performed a series of high-resolution fMRI studies at 3 T to investigate basic visual response properties of the SC. The retinotopic organization of the SC was determined using the traveling wave method with flickering checkerboard stimuli presented at different polar angles and eccentricities. SC activations were confined to stimulation of the contralateral hemifield. Although a detailed retinotopic map was not observed, across subjects, the upper and lower visual fields were represented medially and laterally, respectively. Responses were dominantly evoked by stimuli presented along the horizontal meridian of the visual field. We also measured the sensitivity of the SC to luminance contrast, which has not been previously reported in primates. SC responses were nearly saturated by low contrast stimuli and showed only small response modulation with higher contrast stimuli, indicating high sensitivity to stimulus contrast. Responsiveness to stimulus motion in the SC was shown by robust activations evoked by moving versus static dot stimuli that could not be attributed to eye movements. The responses to contrast and motion stimuli were compared with those in the human lateral geniculate nucleus. Our results provide first insights into basic visual responses of the human SC and show the feasibility of studying subcortical structures using high-resolution fMRI.


2019 ◽  
Author(s):  
Ethan J. Duwell ◽  
Erica N. Woertz ◽  
Jedidiah Mathis ◽  
Joseph Carroll ◽  
Edgar A. DeYoe

ABSTRACTRetinotopic organization is a fundamental feature of visual cortex thought to play a vital role in encoding spatial information. One important aspect of normal retinotopy is the representation of the right and left hemifields in contralateral visual cortex. However, in human albinism, many temporal retinal afferents decussate pathologically at the optic chiasm resulting in partially superimposed representations of opposite hemifields in each hemisphere of visual cortex. Previous fMRI studies in human albinism suggest that the right and left hemifield representations are superimposed in a mirror-symmetric manner. This should produce imaging voxels which respond to two separate regions in visual space mirrored across the vertical meridian. However, it is not yet clear how retino-cortical miswiring in albinism manifests at the level of single voxel population receptive fields. Here we used fMRI retinotopic mapping in conjunction with population receptive field (pRF) modeling to fit both single and dual pRF models to the visual responses of voxels in visual areas V1-V3 of five subjects with albinism. We found that subjects with albinism (but not controls) have sizable clusters of voxels with dual pRFs consistently corresponding to, but not fully coextensive with regions of hemifield overlap. These dual pRFs were typically positioned at roughly mirror image locations across the vertical meridian but were uniquely clustered within the visual field for each subject. We also found that single pRFs are larger in albinism than controls, and that single pRF sizes in the central visual field were anti-correlated with subjects’ foveal cone densities. Finally, dual pRF and aberrant hemifield representation characteristics varied significantly across subjects with albinism suggesting more central heterogeneity than previously appreciated.


1988 ◽  
Vol 60 (1) ◽  
pp. 344-364 ◽  
Author(s):  
T. Sato

1. Extracellular discharges were recorded from neurons in the inferior temporal cortex (area TE) of three macaque monkeys while they performed visual fixation and pattern discrimination tasks. For the pattern discrimination task, monkey was trained to release the lever quickly at the onset of one of two pattern stimuli and to release the lever at the dimming of the other pattern. During this task, neutral light stimulus (light bar) to which the monkey was not required to respond was presented once a trial either prior to the onset of the discriminandum or during presentation of the pattern that dimmed later. The neuronal activities evoked by the neutral stimulus under these two conditions were compared. 2. When the discriminanda were located at the center or at 5 degrees in the contralateral visual field, one-half of the neurons showed significantly smaller responses to the neutral stimulus when it was presented during presentation of the dimming pattern than when it was presented prior to the onset of the discriminandum. 3. The suppressive effect depended on the location of the two stimuli. When the neutral stimulus was located in the ipsilateral visual field and the pattern was located in the contralateral visual field, the response to the neutral stimulus was suppressed. However, when the pattern was located in the ipsilateral visual field (5 degrees visual angle), still within the receptive field for many neurons, the suppressive effect of the pattern on the response to the neutral stimulus in the contralateral visual field was almost undetectable. 4. When the pattern was located nearer the fovea than was the neutral stimulus, the suppressive effect was greater than when the pattern was located more peripherally to the neutral stimulus. Different from the receptive field of more primary visual neurons, this suppressive effect did not appear to be related to the neuron's responsiveness to the patterns nor to precise stimulus location in the receptive field. 5. The magnitude of suppression by the attended pattern on the visual response during the pattern discrimination task correlated with the suppression noted in the presence of a fixation spot during the fixation tasks, while the animals did not fixate on the attended pattern. The response of some neurons to the neutral stimulus prior to pattern presentation during the pattern discrimination task was enhanced slightly compared with the response recorded during the simple fixation task.(ABSTRACT TRUNCATED AT 400 WORDS)


2021 ◽  
Author(s):  
Cornelia Buehlmann ◽  
Paul Graham

ABSTRACTWood ant foragers show an innate attraction to conspicuous visual cues. These foragers inhabit cluttered woodland habitat and feed on honeydew from aphids on trees, hence, the attraction to ‘tree-like’ objects might be an ecologically relevant behaviour that is tailored to wood ant foraging ecology. Foragers from other ant species with different foraging ecologies show innate attractions different to wood ants. What we do not know, however, is whether these innate visual responses vary with the ants’ motivational states or caste. We thus recorded the innate visual response of wood ant foragers with different motivational states, i.e. unfed or fed, as well as males that have a short life span and show no foraging activity. Our results show that ants from all three groups orient towards the visual cue, i.e. the wood ants’ innate visual attraction is not context dependent, but a hardwired behaviour seen across different motivational and ecological contexts.


Biomedicines ◽  
2021 ◽  
Vol 9 (1) ◽  
pp. 77
Author(s):  
Kristin M. Barry ◽  
Donald Robertson ◽  
Wilhelmina H. A. M. Mulders

In the adult auditory system, loss of input resulting from peripheral deafferentation is well known to lead to plasticity in the central nervous system, manifested as reorganization of cortical maps and altered activity throughout the central auditory pathways. The auditory system also has strong afferent and efferent connections with cortico-limbic circuitry including the prefrontal cortex and the question arises whether this circuitry is also affected by loss of peripheral input. Recent studies in our laboratory showed that PFC activation can modulate activity of the auditory thalamus or medial geniculate nucleus (MGN) in normal hearing rats. In addition, we have shown in rats that cochlear trauma resulted in altered spontaneous burst firing in MGN. However, whether the PFC influence on MGN is changed after cochlear trauma is unknown. We investigated the effects of electrical stimulation of PFC on single neuron activity in the MGN in anaesthetized Wistar rats 2 weeks after acoustic trauma or sham surgery. Electrical stimulation of PFC showed a variety of effects in MGN neurons both in sham and acoustic trauma groups but inhibitory responses were significantly larger in the acoustic trauma animals. These results suggest an alteration in functional connectivity between PFC and MGN after cochlear trauma. This change may be a compensatory mechanism increasing sensory gating after the development of altered spontaneous activity in MGN, to prevent altered activity reaching the cortex and conscious perception.


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