Task-relevant Output Signals are Sent from Monkey Dorsolateral Prefrontal Cortex to the Superior Colliculus during a Visuospatial Working Memory Task

Visuospatial working memory is one of the most extensively investigated functions of the dorsolateral prefrontal cortex (DLPFC). Theories of prefrontal cortical function have suggested that this area exerts cognitive control by modulating the activity of structures to which it is connected. Here, we used the oculomotor system as a model in which to characterize the output signals sent from the DLPFC to a target structure during a classical spatial working memory task. We recorded the activity of identified DLPFC–superior colliculus (SC) projection neurons while monkeys performed a memory-guided saccade task in which they were required to generate saccades toward remembered stimulus locations. DLPFC neurons sent signals related to all aspects of the task to the SC, some of which were spatially tuned. These data provide the first direct evidence that the DLPFC sends task-relevant information to the SC during a spatial working memory task, and further support a role for the DLPFC in the direct modulation of other brain areas.

[1]  R. Wurtz,et al.  Frontal eye field neurons orthodromically activated from the superior colliculus. , 1998, Journal of neurophysiology.

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

[3]  R. Wurtz,et al.  Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. , 2000, Journal of neurophysiology.

[4]  R. Douglas,et al.  Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades , 2004, Experimental Brain Research.

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

[6]  C. Pierrot-Deseilligny,et al.  The Role of the Human Dorsolateral Prefrontal Cortex in Ocular Motor Behavior , 2005, Annals of the New York Academy of Sciences.

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

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

[9]  E. J. Tehovnik.  Electrical stimulation of neural tissue to evoke behavioral responses , 1996, Journal of Neuroscience Methods.

[10]  R. Wurtz,et al.  Comparison of cortico-cortical and cortico-collicular signals for the generation of saccadic eye movements. , 2002, Journal of neurophysiology.

[11]  Shintaro Funahashi,et al.  Contributions of prefrontal cue-, delay-, and response-period activity to the decision process of saccade direction in a free-choice ODR task , 2006, Neural Networks.

[12]  Michael E. Goldberg,et al.  Prefrontal Neurons Coding Suppression of Specific Saccades , 2004, Neuron.

[13]  D. Munoz,et al.  Saccadic Probability Influences Motor Preparation Signals and Time to Saccadic Initiation , 1998, The Journal of Neuroscience.

[14]  D. Munoz,et al.  Neuronal Activity in Monkey Superior Colliculus Related to the Initiation of Saccadic Eye Movements , 1997, The Journal of Neuroscience.

[15]  A. Fuchs,et al.  Discharge patterns of neurons in the pretectal nucleus of the optic tract (NOT) in the behaving primate. , 1990, Journal of neurophysiology.

[16]  J. Simpson,et al.  The pretectal nuclear complex and the accessory optic system. , 1988, Reviews of oculomotor research.

[17]  C. Bruce,et al.  Topography of projections to posterior cortical areas from the macaque frontal eye fields , 1995, The Journal of comparative neurology.

[18]  C. Bruce,et al.  Topography of projections to the frontal lobe from the macaque frontal eye fields , 1993, The Journal of comparative neurology.

[19]  J. B. Ranck,et al.  Which elements are excited in electrical stimulation of mammalian central nervous system: A review , 1975, Brain Research.

[20]  R. Wurtz,et al.  Monkey posterior parietal cortex neurons antidromically activated from superior colliculus. , 1997, Journal of neurophysiology.

[21]  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.

[22]  David J. Freedman,et al.  Representation of the Quantity of Visual Items in the Primate Prefrontal Cortex , 2002, Science.

[23]  R. Andersen,et al.  Saccade-related activity in the lateral intraparietal area. II. Spatial properties. , 1991, Journal of neurophysiology.

[24]  C. Bruce,et al.  Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons , 1988, The Journal of comparative neurology.

[25]  R. Wurtz,et al.  Progression in neuronal processing for saccadic eye movements from parietal cortex area lip to superior colliculus. , 2001, Journal of neurophysiology.

[26]  T. Raphan,et al.  Nystagmus induced by stimulation of the nucleus of the optic tract in the monkey , 1988, Experimental Brain Research.

[27]  Stefan Everling,et al.  Neural Activity in Monkey Prefrontal Cortex Is Modulated by Task Context and Behavioral Instruction during Delayed-match-to-sample and Conditional ProsaccadeAntisaccade Tasks , 2006, Journal of Cognitive Neuroscience.

[28]  Tadashi Kawasaki,et al.  Role of the nucleus of the optic tract in monkeys in relation to optokinetic nystagmus , 1986, Brain Research.

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

[30]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[31]  R. Wurtz,et al.  Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. , 1995, Journal of neurophysiology.

[32]  Christos Constantinidis,et al.  A Neural Circuit Basis for Spatial Working Memory , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[33]  P. Goldman-Rakic,et al.  Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex. , 1991, Journal of neurophysiology.

[34]  Masataka Watanabe.  Reward expectancy in primate prefrental neurons , 1996, Nature.

[35]  D. Robinson.  Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

[36]  J. Duncan,et al.  Filtering of neural signals by focused attention in the monkey prefrontal cortex , 2002, Nature Neuroscience.

[37]  D. Sparks,et al.  Dissociation of visual and saccade-related responses in superior colliculus neurons. , 1980, Journal of neurophysiology.

[38]  R. Andersen,et al.  Memory related motor planning activity in posterior parietal cortex of macaque , 1988, Experimental Brain Research.

[39]  D. Munoz,et al.  Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. , 1998, Journal of neurophysiology.

[40]  Walle J. H. Nauta,et al.  Autoradiographic demonstration of a projection from prefrontal association cortex to the superior colliculus in the rhesus monkey , 1976, Brain Research.

[41]  M. Goldberg,et al.  Functional properties of corticotectal neurons in the monkey's frontal eye field. , 1987, Journal of neurophysiology.

[42]  T. Sawaguchi,et al.  Prefrontal cortical representation of visuospatial working memory in monkeys examined by local inactivation with muscimol. , 2001, Journal of neurophysiology.

[43]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[44]  C. Bruce,et al.  Physiological correlate of fixation disengagement in the primate's frontal eye field. , 1994, Journal of neurophysiology.

[45]  J. Lipski,et al.  Antidromic activation of neurones as an analytic tool in the study of the central nervous system , 1981, Journal of Neuroscience Methods.

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

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

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

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

[50]  G. B. Stanton,et al.  Cytoarchitectural characteristic of the frontal eye fields in macaque monkeys , 1989, The Journal of comparative neurology.

[51]  R. Wurtz,et al.  Frontal eye field sends delay activity related to movement, memory, and vision to the superior colliculus. , 2001, Journal of neurophysiology.

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

[53]  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.

[54]  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.

[55]  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.

[56]  R. Wurtz,et al.  Signal transformations from cerebral cortex to superior colliculus for the generation of saccades , 2001, Vision Research.

[57]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[58]  Jerald D. Kralik,et al.  Representation of Attended Versus Remembered Locations in Prefrontal Cortex , 2004, PLoS biology.

[59]  E. Miller,et al.  Neural Activity in the Primate Prefrontal Cortex during Associative Learning , 1998, Neuron.

[60]  T. Duka,et al.  Behavioural measures of frontal lobe function in a population of young social drinkers with binge drinking pattern , 2009, Pharmacology Biochemistry and Behavior.

[61]  P. Goldman-Rakic,et al.  Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. , 1990, Journal of neurophysiology.

[62]  M E Goldberg,et al.  Participation of prefrontal neurons in the preparation of visually guided eye movements in the rhesus monkey. , 1989, Journal of neurophysiology.

[63]  K. Johnston,et al.  Monkey Dorsolateral Prefrontal Cortex Sends Task-Selective Signals Directly to the Superior Colliculus , 2006, The Journal of Neuroscience.

[64]  S. Highstein,et al.  The anatomy and physiology of primate neurons that control rapid eye movements. , 1994, Annual review of neuroscience.

[65]  C. Jacobsen,et al.  Studies of cerebral function in primates. IV. The effects of frontal lobe lesions on the delayed alternation habit in monkeys. , 1937 .

[66]  D. Sparks.  Functional properties of neurons in the monkey superior colliculus: Coupling of neuronal activity and saccade onset , 1978, Brain Research.

[67]  Okihide Hikosaka,et al.  Tonic activity during visuo-oculomotor behavior in the monkey superior colliculus , 1996, Neuroscience Research.

[68]  P. Goldman-Rakic,et al.  Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. , 2000, Journal of neurophysiology.

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

[70]  Stefan Everling,et al.  Rule-dependent Activity for Prosaccades and Antisaccades in the Primate Prefrontal Cortex , 2005, Journal of Cognitive Neuroscience.