Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex.

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)

[1]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[2]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

[3]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

[4]  G. E. Alexander,et al.  Delayed response deficit by cryogenic depression of frontal cortex. , 1970, Brain research.

[5]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[6]  H. Niki,et al.  Prefrontal cortical unit activity and delayed alternation performance in monkeys. , 1971, Journal of neurophysiology.

[7]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[8]  J. Fuster Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. , 1973, Journal of neurophysiology.

[9]  J M Fuster,et al.  Firing changes in cells of the nucleus medialis dorsalis associated with delayed response behavior. , 1973, Brain research.

[10]  H Niki,et al.  Prefrontal unit activity during delayed alternation in the monkey. I. Relation to direction of response. , 1974, Brain research.

[11]  K. Kubota,et al.  Visuokinetic activities of primate prefrontal neurons during delayed-response performance. , 1974, Journal of neurophysiology.

[12]  H. Niki Differential activity of prefrontal units during right and left delayed response trials. , 1974, Brain research.

[13]  H Niki,et al.  Prefrontal unit activity during delayed alternation in the monkey. II. Relation to absolute versus relative direction of response. , 1974, Brain research.

[14]  Mountcastle Vb The world around us: neural command function for selective attention. , 1976 .

[15]  Masataka Watanabe,et al.  Prefrontal unit activity and delayed response: Relation to cue location versus direction of response , 1976, Brain Research.

[16]  Masataka Watanabe,et al.  Cingulate unit activity and delayed response , 1976, Brain Research.

[17]  John Q. Trojanowski,et al.  Prefrontal granular cortex of the rhesus monkey. I. Intrahemispheric cortical afferents , 1977, Brain Research.

[18]  C. Rosenkilde,et al.  Functional heterogeneity of the prefrontal cortex in the monkey: a review. , 1979, Behavioral and neural biology.

[19]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[20]  A. Mikami,et al.  Neuronal activity in the monkey dorsolateral prefrontal cortex during a discrimination task with delay , 1980, Brain Research.

[21]  S. Kojima Prefrontal unit activity in the monkey: Relation to visual stimuli and movements , 1980, Experimental Neurology.

[22]  G. Leichnetz,et al.  The prefrontal corticotectal projection in the monkey; An anterograde and retrograde horseradish peroxidase study , 1981, Neuroscience.

[23]  M. Goldberg,et al.  Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation in frontal eye fields specifically related to saccades. , 1981, Journal of neurophysiology.

[24]  Masataka Watanabe,et al.  Prefrontal unit activity during delayed conditional discriminations in the monkey , 1981, Brain Research.

[25]  Joaquin M. Fuster,et al.  Single cell activity in ventral prefrontal cortex of behaving monkeys , 1981, Brain Research.

[26]  P. Goldman-Rakic,et al.  Delay-related activity of prefrontal neurons in rhesus monkeys performing delayed response , 1982, Brain Research.

[27]  J. Fuster,et al.  Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks , 1982, Experimental Neurology.

[28]  S. Funahashi,et al.  Direction-specific activities of dorsolateral prefrontal and motor cortex pyramidal tract neurons during visual tracking. , 1982, Journal of neurophysiology.

[29]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. , 1983, Journal of neurophysiology.

[30]  Shozo Kojima,et al.  Functional analysis of spatially discriminative neurons in prefrontal cortex of rhesus monkey , 1984, Brain Research.

[31]  D. Pandya,et al.  Projections to the frontal cortex from the posterior parietal region in the rhesus monkey , 1984, The Journal of comparative neurology.

[32]  P S Goldman-Rakic,et al.  Callosal and intrahemispheric connectivity of the prefrontal association cortex in rhesus monkey: Relation between intraparietal and principal sulcal cortex , 1984, The Journal of comparative neurology.

[33]  J. Fuster The Prefrontal Cortex and Temporal Integration , 1985 .

[34]  Hidehiko Komatsu,et al.  Projections from the functional subdivisions of the frontal eye field to the superior colliculus in the monkey , 1985, Brain Research.

[35]  A. S. Batuev,et al.  Comparative characteristics of unit activity in the prefrontal and parietal areas during delayed performance in monkeys , 1985, Behavioural Brain Research.

[36]  C. Bruce,et al.  Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. , 1985, Journal of neurophysiology.

[37]  H. Niki,et al.  Hippocampal unit activity and delayed response in the monkey , 1985, Brain Research.

[38]  P. Goldman-Rakic,et al.  Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  C. Bruce,et al.  Primate frontal eye fields. I. Single neurons discharging before saccades. , 1985, Journal of neurophysiology.

[40]  D. Stuss,et al.  The Frontal Lobes , 1986 .

[41]  Masataka Watanabe,et al.  Prefrontal unit activity during delayed conditional Go/No-go discrimination in the monkey. I. Relation to the stimulus , 1986, Brain Research.

[42]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[43]  Masataka Watanabe,et al.  Prefrontal unit activity during delayed conditional Go/No-go discrimination in the monkey. II. Relation to Go and No-go responses , 1986, Brain Research.

[44]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[45]  P. Goldman-Rakic,et al.  Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  P. Goldman-Rakic Topography of cognition: parallel distributed networks in primate association cortex. , 1988, Annual review of neuroscience.

[47]  G. F. Tremblay,et al.  The Prefrontal Cortex , 1989, Neurology.