Rule‐dependent shifting of sensorimotor representation in the primate prefrontal cortex

When we react to the outer world, perceived sensory information is frequently memorized over a temporal interval then transformed into a motor command based on a behavioural rule. In this type of memory‐based sensorimotor transformation, working memory is considered to play an important role. It has been suggested that the lateral prefrontal cortex is involved in the process of the working memory. However, the neuronal mechanism for guiding a motor command from the working memory has not been established. To examine how visuospatial working memory is linked with a forthcoming saccade direction, we used an antisaccade paradigm for monkeys in which a behavioural rule was presented in the middle of a delay period. In this task, the subjects were required to maintain cue location and to select a response based on a behavioural rule. We found that a subset of mnemonic neurons in the lateral prefrontal cortex changed their representation from cue to saccade direction. Furthermore, the discriminability for saccade direction of these neurons tended to appear soon after the behavioural rule presentation, indicating their significant dependency on the behavioural rule. These results suggest that a subset of mnemonic neurons in the lateral prefrontal cortex change their activity depending on a behavioural rule to guide a prospective motor command.

[1]  C. Jacobsen FUNCTIONS OF FRONTAL ASSOCIATION AREA IN PRIMATES , 1935 .

[2]  S. Tsujimoto,et al.  Neuronal representation of response-outcome in the primate prefrontal cortex. , 2004, Cerebral cortex.

[3]  S. Funahashi,et al.  Population vector analysis of primate prefrontal activity during spatial working memory. , 2004, Cerebral cortex.

[4]  P. Goldman-Rakic Cellular basis of working memory , 1995, Neuron.

[5]  R. Passingham,et al.  The prefrontal cortex: response selection or maintenance within working memory? , 2000, 5th IEEE EMBS International Summer School on Biomedical Imaging, 2002..

[6]  J. Fuster,et al.  Delayed-matching and delayed-response deficit from cooling dorsolateral prefrontal cortex in monkeys. , 1976, Journal of comparative and physiological psychology.

[7]  S. Wise,et al.  Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  Jun Zhang,et al.  Flexible filaments in a flowing soap film as a model for one-dimensional flags in a two-dimensional wind , 2000, Nature.

[9]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[10]  T. Sawaguchi,et al.  Contrasting effects of reward expectation on sensory and motor memories in primate prefrontal neurons. , 2006, Cerebral cortex.

[11]  Alexandre Pouget,et al.  Computational approaches to sensorimotor transformations , 2000, Nature Neuroscience.

[12]  J. Tanji,et al.  Neuronal activity in the primate prefrontal cortex in the process of motor selection based on two behavioral rules. , 2000, Journal of neurophysiology.

[13]  P. Goldman-Rakic,et al.  Destruction and Creation of Spatial Tuning by Disinhibition: GABAA Blockade of Prefrontal Cortical Neurons Engaged by Working Memory , 2000, The Journal of Neuroscience.

[14]  T. Sawaguchi,et al.  Monkey prefrontal neuronal activity coding the forthcoming saccade in an oculomotor delayed matching-to-sample task. , 1998, Journal of neurophysiology.

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

[16]  M. Schlag-Rey,et al.  Antisaccade performance predicted by neuronal activity in the supplementary eye field , 1997, Nature.

[17]  J. Tanji,et al.  Integration of temporal order and object information in the monkey lateral prefrontal cortex. , 2004, Journal of neurophysiology.

[18]  E. Miller,et al.  From rule to response: neuronal processes in the premotor and prefrontal cortex. , 2003, Journal of neurophysiology.

[19]  P. Goldman-Rakic,et al.  Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. , 2000, Cerebral cortex.

[20]  E. Zarahn,et al.  The Role of Prefrontal Cortex in Sensory Memory and Motor Preparation: An Event-Related fMRI Study , 2000, NeuroImage.

[21]  Mingsha Zhang,et al.  Neuronal switching of sensorimotor transformations for antisaccades , 2000, Nature.

[22]  Shintaro Funahashi,et al.  Prefrontal task-related activity representing visual cue location or saccade direction in spatial working memory tasks. , 2002, Journal of neurophysiology.

[23]  Shabtai Barash,et al.  Paradoxical activities: insight into the relationship of parietal and prefrontal cortices , 2003, Trends in Neurosciences.

[24]  Kenichi Ohki,et al.  Conversion of Working Memory to Motor Sequence in the Monkey Premotor Cortex , 2003, Science.

[25]  J. Hanley,et al.  The meaning and use of the area under a receiver operating characteristic (ROC) curve. , 1982, Radiology.

[26]  Okihide Hikosaka,et al.  A Code for Behavioral Inhibition on the Basis of Color, But Not Motion, in Ventrolateral Prefrontal Cortex of Macaque Monkey , 2001, The Journal of Neuroscience.

[27]  P. Goldman-Rakic,et al.  Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task , 1993, Nature.

[28]  Modular activation, and suppression of neocortical activity in the monkey revealed by optical imaging , 1994, Neuroreport.

[29]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[30]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[31]  D P Munoz,et al.  Neuronal Correlates for Preparatory Set Associated with Pro-Saccades and Anti-Saccades in the Primate Frontal Eye Field , 2000, The Journal of Neuroscience.

[32]  P. Goldman-Rakic,et al.  Areal segregation of face-processing neurons in prefrontal cortex. , 1997, Science.

[33]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[34]  D Le Bihan,et al.  The Dorsolateral Prefrontal Cortex (dlpfc) Plays a Key Role in Working Memory (wm). yet Its Precise Contribution , 2022 .

[35]  P. E. Hallett,et al.  Primary and secondary saccades to goals defined by instructions , 1978, Vision Research.

[36]  Christos Constantinidis,et al.  The sensory nature of mnemonic representation in the primate prefrontal cortex , 2001, Nature Neuroscience.

[37]  J. Tanji,et al.  Behavioral planning in the prefrontal cortex , 2001, Current Opinion in Neurobiology.

[38]  P. Goldman-Rakic,et al.  Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas" , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  T. Sawaguchi,et al.  Properties of delay-period neuronal activity in the monkey dorsolateral prefrontal cortex during a spatial delayed matching-to-sample task. , 1999, Journal of neurophysiology.

[40]  Christopher A. Buneo,et al.  Direct visuomotor transformations for reaching , 2002, Nature.

[41]  N. P. Bichot,et al.  Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. , 1996, Journal of neurophysiology.

[42]  Mingsha Zhang,et al.  Persistent LIP activity in memory antisaccades: working memory for a sensorimotor transformation. , 2004, Journal of neurophysiology.

[43]  J. Kalaska,et al.  Simultaneous encoding of multiple potential reach directions in dorsal premotor cortex. , 2002, Journal of neurophysiology.

[44]  Emilio Salinas,et al.  Background Synaptic Activity as a Switch Between Dynamical States in a Network , 2003, Neural Computation.

[45]  M. Shadlen,et al.  Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque , 1999, Nature Neuroscience.

[46]  M. Goldberg,et al.  Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task , 1999, Nature Neuroscience.

[47]  H. E. Rosvold,et al.  Localization of function within the dorsolateral prefrontal cortex of the rhesus monkey. , 1970, Experimental neurology.

[48]  P. Goldman-Rakic,et al.  A role for inhibition in shaping the temporal flow of information in prefrontal cortex , 2002, Nature Neuroscience.

[49]  J. Fuster,et al.  From perception to action: temporal integrative functions of prefrontal and parietal neurons. , 1999, Cerebral cortex.

[50]  S. Everling,et al.  The antisaccade: a review of basic research and clinical studies , 1998, Neuropsychologia.

[51]  S. P. Wise,et al.  Primate frontal cortex: effects of stimulus and movement , 2004, Experimental Brain Research.

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

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

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

[55]  D P Munoz,et al.  Role of Primate Superior Colliculus in Preparation and Execution of Anti-Saccades and Pro-Saccades , 1999, The Journal of Neuroscience.