Enhanced modulation of neuronal activity during antisaccades in the primate globus pallidus.

The antisaccade task has been widely used to investigate the neural mechanisms underlying volitional movement control. In this task, subjects suppress reflexive saccades to the sudden appearance of peripheral visual stimuli (prosaccades) and generate a saccade in the opposite direction. Recent imaging studies suggest that the globus pallidus (GP) is involved in the generation of antisaccades. To understand the roles of the GP, we examined single neuron activity and the effects of local inactivation. Monkeys were trained to make either a pro- or antisaccade according to prior instruction provided by the color of the fixation point in each trial. Among 119 saccade-related neurons, 55% showed increased firing rates associated with saccades, whereas the remaining neurons showed decreased firing rates. For both populations of neurons, the activity modulation was enhanced during the preparation and execution of antisaccades, as compared with prosaccades. Inactivation of the recording sites in the external segment of the GP resulted in an increase in the number of error trials in the antisaccade tasks, suggesting that signals in the GP may play roles in suppressing inadequate prosaccades in the task. Signals in the GP might regulate eye movements through the nigro-collicular descending circuitry and through the basal ganglia-thalamocortical pathways.

[1]  J Schlag,et al.  Primate supplementary eye field. II. Comparative aspects of connections with the thalamus, corpus striatum, and related forebrain nuclei , 1991, The Journal of comparative neurology.

[2]  B. Stein,et al.  Opposing basal ganglia processes shape midbrain visuomotor activity bilaterally , 2003, Nature.

[3]  Garrett E. Alexander Basal ganglia , 1998 .

[4]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[5]  R. Wurtz,et al.  Modification of saccadic eye movements by GABA-related substances. II. Effects of muscimol in monkey substantia nigra pars reticulata. , 1985, Journal of neurophysiology.

[6]  A. Berthoz,et al.  PET study of voluntary saccadic eye movements in humans: basal ganglia-thalamocortical system and cingulate cortex involvement. , 1993, Journal of neurophysiology.

[7]  A. Straube,et al.  Electrical stimulation of the posteroventral pallidum influences internally guided saccades in Parkinson’s disease , 1998, Journal of Neurology.

[8]  Madeleine Schlag-Rey,et al.  Primate antisaccade. II. Supplementary eye field neuronal activity predicts correct performance. , 2004, Journal of neurophysiology.

[9]  H. Komatsu,et al.  Effects of task demands on the responses of color-selective neurons in the inferior temporal cortex , 2007, Nature Neuroscience.

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

[11]  M. D’Esposito,et al.  Frontal Networks for Learning and Executing Arbitrary Stimulus-Response Associations , 2005, The Journal of Neuroscience.

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

[13]  Ivan Toni,et al.  Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: a PET study , 1999, Experimental Brain Research.

[14]  Masaki Tanaka,et al.  Inactivation of the central thalamus delays self-timed saccades , 2006, Nature Neuroscience.

[15]  O. Hikosaka,et al.  Function of the Indirect Pathway in the Basal Ganglia Oculomotor System: Visuo-Oculomotor Activities of External Pallidum Neurons , 1995 .

[16]  M Vidailhet,et al.  Mixing pro- and antisaccades in patients with parkinsonian syndromes. , 2006, Brain : a journal of neurology.

[17]  松田 哲也,et al.  Functional MRI mapping of brain activation during visually guided saccades and antisaccades : cortical and subcortical networks , 2004 .

[18]  R. Wurtz,et al.  Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus. , 1985, Journal of neurophysiology.

[19]  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.

[20]  O. Hikosaka,et al.  Switching from automatic to controlled action by monkey medial frontal cortex , 2007, Nature Neuroscience.

[21]  A. Parent,et al.  Contralateral pallidothalamic and pallidotegmental projections in primates: an anterograde and retrograde labeling study , 1991, Brain Research.

[22]  Stephen G Lisberger,et al.  Medial Versus Lateral Frontal Lobe Contributions to Voluntary Saccade Control as Revealed by the Study of Patients with Frontal Lobe Degeneration , 2006, The Journal of Neuroscience.

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

[24]  G. Pari,et al.  Saccadic impairments in Huntington’s disease , 2008, Experimental Brain Research.

[25]  Masaki Tanaka,et al.  Smooth Pursuit Eye Movements , 2018 .

[26]  M. Schlag-Rey,et al.  Primate antisaccades. I. Behavioral characteristics. , 1998, Journal of neurophysiology.

[27]  P. Tu,et al.  Neural correlates of antisaccade deficits in schizophrenia, an fMRI study. , 2006, Journal of psychiatric research.

[28]  S B Edwards,et al.  A comparison of the intranigral distribution of nigrotectal neurons labeled with horseradish peroxidase in the monkey, cat, and rat , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  E. Miller,et al.  Different time courses of learning-related activity in the prefrontal cortex and striatum , 2005, Nature.

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

[31]  P. Strick,et al.  Basal-ganglia 'projections' to the prefrontal cortex of the primate. , 2002, Cerebral cortex.

[32]  J. Lynch,et al.  Corticocortical input to the smooth and saccadic eye movement subregions of the frontal eye field in Cebus monkeys. , 1996, Journal of neurophysiology.

[33]  Y. Agid,et al.  Saccade disturbances after bilateral lentiform nucleus lesions in humans. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[34]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[35]  Masaki Tanaka,et al.  Cognitive Signals in the Primate Motor Thalamus Predict Saccade Timing , 2007, The Journal of Neuroscience.

[36]  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.

[37]  G. Pari,et al.  Deficits in saccadic eye-movement control in Parkinson's disease , 2005, Neuropsychologia.

[38]  D. Surmeier,et al.  Striatal Information Signaling and Integration in Globus Pallidus: Timing Matters , 2006, Neurosignals.

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

[40]  J. Lynch,et al.  Subcortical Input to the Smooth and Saccadic Eye Movement Subregions of the Frontal Eye Field in Cebus Monkey , 1997, The Journal of Neuroscience.

[41]  A. Parent,et al.  Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidium in basal ganglia circuitry , 1995, Brain Research Reviews.

[42]  M. Merello,et al.  [Functional anatomy of the basal ganglia]. , 2000, Revista de neurologia.

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

[44]  O. Hikosaka,et al.  Role of the basal ganglia in the control of purposive saccadic eye movements. , 2000, Physiological reviews.

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

[46]  Léon Tremblay,et al.  Antisaccade deficit after inactivation of the principal sulcus in monkeys. , 2006, Cerebral cortex.

[47]  S. Wise,et al.  Comparison of learning‐related neuronal activity in the dorsal premotor cortex and striatum , 2004, The European journal of neuroscience.

[48]  M. Delong,et al.  Activity of pallidal neurons during movement. , 1971, Journal of neurophysiology.

[49]  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.

[50]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

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

[52]  D. Levy,et al.  Functional neuroanatomy of antisaccade eye movements investigated with positron emission tomography. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

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

[54]  A. Lang,et al.  Pallidal deep brain stimulation influences both reflexive and voluntary saccades in Huntington's disease , 2005, Movement disorders : official journal of the Movement Disorder Society.