Nonhuman primate event-related potentials associated with pro- and anti-saccades

Non-invasive event-related potential (ERP) recordings have become a popular technique to study neural activity associated with saccades in humans. To date, it is not known whether nonhuman primates exhibit similar saccade-related ERPs. Here, we recorded ERPs associated with the performance of randomly interleaved pro- and anti-saccades in macaque monkeys. Stimulus-aligned ERPs showed short-latency visual component with more negative P2 and N2 peak amplitudes on anti- than on pro-saccade trials. Saccade-aligned ERPs showed a larger presaccadic negativity on anti- than pro-saccade trials, and a presaccadic positivity on pro-saccade trials, which was attenuated or absent on anti-saccade trials. This was followed by sharp negative spike potential immediately prior to the movement. Overall, these findings demonstrate that macaque monkeys, like humans, exhibit task-related differences of visual ERPs associated with pro- and anti-saccades and furthermore share presaccadic positivity as well as a spike potential prior to these tasks. We suggest that the presaccadic positivity on pro-saccade trials is generated by a source in the contralateral frontal eye fields and that the more negative voltage on anti-saccade trials is the result of additional sources of opposite polarity in neighboring frontal areas.

[1]  A. Fuchs,et al.  Activity of brain stem neurons during eye movements of alert monkeys. , 1972, Journal of neurophysiology.

[2]  A. Engel,et al.  Invasive recordings from the human brain: clinical insights and beyond , 2005, Nature Reviews Neuroscience.

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

[4]  D. Ferrier The Functions of the Brain , 1887, Edinburgh Medical Journal.

[5]  C. M. Davis,et al.  Cerebral Potentials Preceding Visually Triggered Saccades , 1984, Annals of the New York Academy of Sciences.

[6]  Matthew R. G. Brown,et al.  Neural processes associated with antisaccade task performance investigated with event-related FMRI. , 2005, Journal of neurophysiology.

[7]  D. Munoz,et al.  Look away: the anti-saccade task and the voluntary control of eye movement , 2004, Nature Reviews Neuroscience.

[8]  E. Keller Participation of medial pontine reticular formation in eye movement generation in monkey. , 1974, Journal of neurophysiology.

[9]  G. Thickbroom,et al.  Presaccadic ‘spike’ potential: Investigation of topography and source , 1985, Brain Research.

[10]  Richard P. Heitz,et al.  On the origin of event-related potentials indexing covert attentional selection during visual search. , 2009, Journal of neurophysiology.

[11]  A. Starr,et al.  Task-relevant late positive component of the auditory event-related potential in monkeys resembles P300 in humans. , 1984, Science.

[12]  David L. Sparks,et al.  Response properties of eye movement-related neurons in the monkey superior colliculus , 1975, Brain Research.

[13]  I. Evdokimidis,et al.  Cortical potentials preceding centrifugal and centripetal self-paced horizontal saccades. , 1991, Electroencephalography and clinical neurophysiology.

[14]  K. Johnston,et al.  Top-Down Control-Signal Dynamics in Anterior Cingulate and Prefrontal Cortex Neurons following Task Switching , 2007, Neuron.

[15]  Wolfgang Becker,et al.  Bereitschaftspotential, prämotorische Positivierung und andere Hirnpotentiale bei sakkadischen Augenbewegungen , 1972 .

[16]  E. Evarts Pyramidal tract activity associated with a conditioned hand movement in the monkey. , 1966, Journal of neurophysiology.

[17]  R. Wurtz Response of striate cortex neurons to stimuli during rapid eye movements in the monkey. , 1969, Journal of neurophysiology.

[18]  Y. Miyashita,et al.  Functional Magnetic Resonance Imaging of Macaque Monkeys Performing Visually Guided Saccade Tasks Comparison of Cortical Eye Fields with Humans , 2004, Neuron.

[19]  Anders M. Dale,et al.  Repeated fMRI Using Iron Oxide Contrast Agent in Awake, Behaving Macaques at 3 Tesla , 2002, NeuroImage.

[20]  Carey D. Balaban,et al.  The human pre-saccadic spike potential: Influences of a visual target, saccade direction, electrode laterality and instructions to perform saccades , 1985, Brain Research.

[21]  Stefan Everling,et al.  Frontoparietal activation with preparation for antisaccades. , 2007, Journal of neurophysiology.

[22]  A. Mikami,et al.  Functional brain mapping of the macaque related to spatial working memory as revealed by PET. , 2004, Cerebral cortex.

[23]  G. Goldberg,et al.  Topography of scalp potentials preceding self‐initiated saccades , 1990, Neurology.

[24]  V. Mountcastle,et al.  THE FUNCTIONAL PROPERTIES OF VENTROBASAL THALAMIC NEURONSSTUDIED IN UNANESTHETIZED MONKEYS. , 1963, Journal of neurophysiology.

[25]  T. Paus Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[26]  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.

[27]  J. Rohrbaugh,et al.  Cortical and subcortical visual evoked potential correlates of reaction time in monkeys. , 1976, Journal of comparative and physiological psychology.

[28]  C. Schroeder,et al.  Striate cortical contribution to the surface-recorded pattern-reversal vep in the alert monkey , 1991, Vision Research.

[29]  T. Albright,et al.  fMRI of Monkey Visual Cortex , 1998, Neuron.

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

[31]  A. Fuchs,et al.  Firing patterns of abducens neurons of alert monkeys in relationship to horizontal eye movement. , 1970, Journal of neurophysiology.

[32]  Christoph Klein,et al.  Impaired modulation of the saccadic contingent negative variation preceding antisaccades in schizophrenia , 2000, Biological Psychiatry.

[33]  Ravi S. Menon,et al.  Comparison of memory- and visually guided saccades using event-related fMRI. , 2004, Journal of neurophysiology.

[34]  G. Thickbroom,et al.  Cerebral events preceding self-paced and visually triggered saccades. A study of presaccadic potentials. , 1985, Electroencephalography and clinical neurophysiology.

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

[36]  Herbert G. Vaughan,et al.  Relationship of neuronal activity to gross movement-related potentials in monkey pre- and postcentral cortex , 1977, Brain Research.

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

[38]  Jeffrey D Schall,et al.  Nonhuman primate event-related potentials indexing covert shifts of attention , 2007, Proceedings of the National Academy of Sciences.

[39]  Jonathan O. Dostrovsky,et al.  Eye movement-related responses of neurons in human subthalamic nucleus , 2005, Experimental Brain Research.

[40]  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.

[41]  I. Evdokimidis,et al.  Cortical potentials with antisaccades. , 1996, Electroencephalography and clinical neurophysiology.

[42]  Maurizio Corbetta,et al.  Distribution of activity across the monkey cerebral cortical surface, thalamus and midbrain during rapid, visually guided saccades. , 2006, Cerebral cortex.

[43]  R H Wurtz,et al.  Organization of monkey superior colliculus: intermediate layer cells discharging before eye movements. , 1976, Journal of neurophysiology.

[44]  S. Everling,et al.  Cortical potentials preceding pro- and antisaccades in man. , 1997, Electroencephalography and clinical neurophysiology.

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

[46]  C. Curtis,et al.  Success and Failure Suppressing Reflexive Behavior , 2003, Journal of Cognitive Neuroscience.

[47]  A. Toga,et al.  The Rhesus Monkey Brain in Stereotaxic Coordinates , 1999 .

[48]  A. Fuchs,et al.  Eye movements evoked by stimulation of frontal eye fields. , 1969, Journal of neurophysiology.

[49]  A. Mirsky,et al.  Evoked potential correlates of stimulation-induced impairment of attention in Macaca mulatta , 1977, Experimental Neurology.

[50]  T. Mergner,et al.  Dependence of presaccadic cortical potentials on the type of saccadic eye movement. , 1992, Electroencephalography and clinical neurophysiology.

[51]  Diane Kurtzberg,et al.  Topographic analysis of human cortical potentials preceding self-initiated and visually triggered saccades , 1982, Brain Research.

[52]  Theodore Holmes Bullock,et al.  Have Brain Dynamics Evolved? Should We Look for Unique Dynamics in the Sapient Species? , 2003, Neural Computation.

[53]  H. Kornhuber,et al.  [Readiness potential, pre-motor positivity and other changes of cortical potential in saccadic eye movements]. , 1972, Vision Research.

[54]  D. Heeger,et al.  In this issue , 2002, Nature Reviews Drug Discovery.

[55]  R. Wurtz,et al.  Visual receptive fields of frontal eye field neurons. , 1973, Brain research.

[56]  D H Hubel,et al.  Brain mechanisms of vision. , 1979, Scientific American.

[57]  N. Logothetis,et al.  Functional imaging of the monkey brain , 1999, Nature Neuroscience.

[58]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[59]  Kristen A. Ford,et al.  BOLD fMRI activation for anti-saccades in nonhuman primates , 2009, NeuroImage.

[60]  J. DeSouza,et al.  Neural correlates for preparatory set associated with pro-saccades and anti-saccades in humans investigated with event-related fMRI , 2010 .

[61]  M. Ghilardi,et al.  P300-like potentials in the normal monkey using classical conditioning and an auditory 'oddball' paradigm. , 1986, Electroencephalography and clinical neurophysiology.

[62]  C. Scudder,et al.  The microscopic anatomy and physiology of the mammalian saccadic system , 1996, Progress in Neurobiology.