Dissociating the Contributions of Frontal Eye Field Activity to Spatial Working Memory and Motor Preparation

Neurons within dorsolateral prefrontal cortex of primates are characterized by robust persistent spiking activity exhibited during the delay period of working memory tasks. This includes the frontal eye field (FEF) where nearly half of the neurons are active when spatial locations are held in working memory. Past evidence has established the FEF’s contribution to the planning and triggering of saccadic eye movements as well as to the control of visual spatial attention. However, it remains unclear if persistent delay activity reflects a similar dual role in movement planning and visuospatial working memory. We trained monkeys to alternate between different forms of a spatial working memory task which could dissociate remembered stimulus locations from planned eye movements. We tested the effects of inactivation of FEF sites on behavioral performance in the different tasks. Consistent with previous studies, FEF inactivation impaired the execution of memory-guided saccades, and impaired performance when remembered locations matched the planned eye movement. In contrast, memory performance was largely unaffected when the remembered location was dissociated from the correct eye movement response. Overall, the inactivation effects demonstrated clear deficits on eye movements, regardless of task type, but little or no evidence of a deficit in spatial working memory. Thus, our results indicate that persistent delay activity in the FEF contributes primarily to the preparation of eye movements and not to spatial working memory.

[1]  S. Wise,et al.  Evolution of prefrontal cortex , 2021, Neuropsychopharmacology.

[2]  Justin M. Fine,et al.  The whole prefrontal cortex is premotor cortex , 2021, Philosophical Transactions of the Royal Society B.

[3]  Tirin Moore,et al.  Working memory gates visual input to primate prefrontal neurons , 2020, bioRxiv.

[4]  H. Deubel,et al.  Saccade selection and inhibition: motor and attentional components. , 2019, Journal of neurophysiology.

[5]  Hidehiko K. Inagaki,et al.  Discrete attractor dynamics underlies persistent activity in the frontal cortex , 2019, Nature.

[6]  Donatas Jonikaitis,et al.  The interdependence of attention, working memory and gaze control: behavior and neural circuitry. , 2019, Current opinion in psychology.

[7]  Christos Constantinidis,et al.  Persistent Spiking Activity Underlies Working Memory , 2018, The Journal of Neuroscience.

[8]  K. Svoboda,et al.  Neural mechanisms of movement planning: motor cortex and beyond , 2018, Current Opinion in Neurobiology.

[9]  Brian D Corneil,et al.  Frontal Eye Field Inactivation Diminishes Superior Colliculus Activity, But Delayed Saccadic Accumulation Governs Reaction Time Increases , 2017, The Journal of Neuroscience.

[10]  Tirin Moore,et al.  Spatial working memory alters the efficacy of input to visual cortex , 2017, Nature Communications.

[11]  Edward S Boyden,et al.  FEF inactivation with improved optogenetic methods , 2016, Proceedings of the National Academy of Sciences.

[12]  Heiner Deubel,et al.  Oculomotor selection underlies feature retention in visual working memory. , 2016, Journal of neurophysiology.

[13]  Tirin Moore,et al.  A Distinct Contribution of the Frontal Eye Field to the Visual Representation of Saccadic Targets , 2014, The Journal of Neuroscience.

[14]  Tirin Moore,et al.  Persistent Spatial Information in the Frontal Eye Field during Object-Based Short-Term Memory , 2012, The Journal of Neuroscience.

[15]  R. Passingham,et al.  The Neurobiology of the Prefrontal Cortex: Anatomy, Evolution, and the Origin of Insight , 2012 .

[16]  Daeyeol Lee,et al.  Neuronal basis of age-related working memory decline , 2011, Nature.

[17]  Tirin Moore,et al.  A reliable microinjectrode system for use in behaving monkeys , 2011, Journal of Neuroscience Methods.

[18]  Byron M. Yu,et al.  Roles of monkey premotor neuron classes in movement preparation and execution. , 2010, Journal of neurophysiology.

[19]  Tirin Moore,et al.  Selection and Maintenance of Spatial Information by Frontal Eye Field Neurons , 2009, The Journal of Neuroscience.

[20]  Ilya E. Monosov,et al.  Frontal eye field activity enhances object identification during covert visual search. , 2009, Journal of neurophysiology.

[21]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[22]  P. Roelfsema,et al.  Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex , 2008, Science.

[23]  R. Wurtz,et al.  Brain circuits for the internal monitoring of movements. , 2008, Annual review of neuroscience.

[24]  C. Curtis Prefrontal and parietal contributions to spatial working memory , 2006, Neuroscience.

[25]  Takashi R Sato,et al.  Neuronal Basis of Covert Spatial Attention in the Frontal Eye Field , 2005, The Journal of Neuroscience.

[26]  Lawrence H Snyder,et al.  Delay-period activity in visual, visuomovement, and movement neurons in the frontal eye field. , 2005, Journal of neurophysiology.

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

[28]  Katherine M. Armstrong,et al.  Visuomotor Origins of Covert Spatial Attention , 2003, Neuron.

[29]  Ralf Engbert,et al.  Microsaccades uncover the orientation of covert attention , 2003, Vision Research.

[30]  Katherine M. Armstrong,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2003, Nature.

[31]  Frans W Cornelissen,et al.  The Eyelink Toolbox: Eye tracking with MATLAB and the Psychophysics Toolbox , 2002, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[32]  David J. Freedman,et al.  The prefrontal cortex: categories, concepts and cognition. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[33]  T Moore,et al.  Control of eye movements and spatial attention. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[34]  J. Kalaska,et al.  Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity. , 2000, Journal of neurophysiology.

[35]  Joaquín M. Fuster,et al.  Executive frontal functions , 2000, Experimental Brain Research.

[36]  S. Wise,et al.  Rule-dependent neuronal activity in the prefrontal cortex , 1999, Experimental Brain Research.

[37]  M. Segraves,et al.  Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades. , 1999, Journal of neurophysiology.

[38]  Edward J. Tehovnik,et al.  Reversible inactivation of macaque frontal eye field , 1997, Experimental Brain Research.

[39]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[40]  J. Bullier,et al.  Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

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

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

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

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

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

[48]  B. Fischer,et al.  Saccadic eye movements after extremely short reaction times in the monkey , 1983, Brain Research.

[49]  Peter H. Schiller,et al.  The effect of superior colliculus ablation on saccades elicted by cortical stimulation , 1977, Brain Research.

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

[51]  V. Mountcastle,et al.  Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. , 1975, Journal of neurophysiology.

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

[53]  K. Pribram,et al.  Analysis of the effects of frontal lesions in monkey. I. Variations of delayed alternation. , 1955, Journal of comparative and physiological psychology.

[54]  T. Moore,et al.  Microstimulation of the frontal eye field and its effects on covert spatial attention. , 2004, Journal of neurophysiology.

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

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

[57]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.