Modeling the role of basal ganglia in saccade generation: Is the indirect pathway the explorer?

We model the role played by the Basal Ganglia (BG) in the generation of voluntary saccadic eye movements. The BG model explicitly represents key nuclei like the striatum (caudate), Substantia Nigra pars reticulata (SNr) and compata (SNc), the Subthalamic Nucleus (STN), the two pallidal nuclei and Superior Colliculus. The model is cast within the Reinforcement Learning (RL) framework, with the dopamine representing the temporal difference error, the striatum serving as the critic, and the indirect pathway playing the role of the explorer. Performance of the model is evaluated on a set of tasks such as feature and conjunction searches, directional selectivity and a successive saccade task. Behavioral phenomena such as independence of search time on number of distractors in feature search and linear increase in search time with number of distractors in conjunction search are observed. It is also seen that saccadic reaction times are longer and search efficiency is impaired on diminished BG contribution, which corroborates with reported data obtained from Parkinson's Disease (PD) patients.

[1]  O. Hikosaka,et al.  Role for Subthalamic Nucleus Neurons in Switching from Automatic to Controlled Eye Movement , 2008, The Journal of Neuroscience.

[2]  Kae Nakamura,et al.  Basal ganglia orient eyes to reward. , 2006, Journal of neurophysiology.

[3]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. , 1983, Journal of neurophysiology.

[4]  A. Cooper,et al.  Predictive Reward Signal of Dopamine Neurons , 2011 .

[5]  D. Willshaw,et al.  Subthalamic–pallidal interactions are critical in determining normal and abnormal functioning of the basal ganglia , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  Eytan Ruppin,et al.  Actor-critic models of the basal ganglia: new anatomical and computational perspectives , 2002, Neural Networks.

[7]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

[8]  佐藤 真琴,et al.  Role of primate substantia nigra pars reticulata in reward-oriented saccadic eye movement , 2002 .

[9]  O. Hikosaka,et al.  Eye movements in monkeys with local dopamine depletion in the caudate nucleus. I. Deficits in spontaneous saccades , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  Peter Redgrave,et al.  Basal Ganglia , 2020, Encyclopedia of Autism Spectrum Disorders.

[11]  Michael J. Frank,et al.  Dynamic Dopamine Modulation in the Basal Ganglia: A Neurocomputational Account of Cognitive Deficits in Medicated and Nonmedicated Parkinsonism , 2005, Journal of Cognitive Neuroscience.

[12]  Bruno A. Olshausen,et al.  Book Review , 2003, Journal of Cognitive Neuroscience.

[13]  Peter Ford Dominey,et al.  A cortico-subcortical model for generation of spatially accurate sequential saccades. , 1992, Cerebral cortex.

[14]  H. Kornhuber,et al.  Natural and drug-induced variations of velocity and duration of human saccadic eye movements: Evidence for a control of the neural pulse generator by local feedback , 2004, Biological Cybernetics.

[15]  O. Rascol,et al.  Square wave jerks in parkinsonian syndromes. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[16]  V. Srinivasa Chakravarthy,et al.  Understanding Parkinsonian Handwriting Through a Computational Model of Basal Ganglia , 2008, Neural Computation.

[17]  Charles J. Wilson,et al.  Activity Patterns in a Model for the Subthalamopallidal Network of the Basal Ganglia , 2002, The Journal of Neuroscience.

[18]  V. S. Chakravarthy,et al.  The Role of the Basal Ganglia in Exploration in a Neural Model Based on Reinforcement Learning , 2006, Int. J. Neural Syst..

[19]  P. Bach-y-Rita,et al.  Basic Mechanisms of Ocular Motility and Their Clinical Implications , 1976 .

[20]  Philippe Lefèvre,et al.  Dynamic feedback to the superior colliculus in a neural network model of the gaze control system , 1992, Neural Networks.

[21]  Kenji Doya,et al.  Metalearning and neuromodulation , 2002, Neural Networks.

[22]  D. Heeger Modeling simple-cell direction selectivity with normalized, half-squared, linear operators. , 1993, Journal of neurophysiology.

[23]  O. Hikosaka,et al.  Expectation of reward modulates cognitive signals in the basal ganglia , 1998, Nature Neuroscience.

[24]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 1998, IEEE Trans. Neural Networks.

[25]  M. A. Basso,et al.  Neuronal Activity in Substantia Nigra Pars Reticulata during Target Selection , 2002, The Journal of Neuroscience.

[26]  Thomas P. Trappenberg,et al.  Modelling divided visual attention with a winner-take-all network , 2005, Neural Networks.

[27]  G. Aston-Jones,et al.  Locus coeruleus neurons in monkey are selectively activated by attended cues in a vigilance task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  Kuniharu Arai,et al.  Two-dimensional neural network model of the primate saccadic system , 1994, Neural Networks.

[29]  V. Russell,et al.  Regional distribution of monoamines and dopamine D1-and D2-receptors in the striatum of the rat , 1992, Neurochemical Research.

[30]  A. Roberts,et al.  Neurons, Networks and Motor Behaviour , 1997 .

[31]  A. Oliviero,et al.  Dopamine Dependency of Oscillations between Subthalamic Nucleus and Pallidum in Parkinson's Disease , 2001, The Journal of Neuroscience.

[32]  D. Surmeier,et al.  Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. , 1998, Advances in pharmacology.

[33]  P. Redgrave,et al.  The basal ganglia: a vertebrate solution to the selection problem? , 1999, Neuroscience.

[34]  P. Dayan,et al.  Cortical substrates for exploratory decisions in humans , 2006, Nature.

[35]  Peter Dayan,et al.  Bee foraging in uncertain environments using predictive hebbian learning , 1995, Nature.

[36]  J. Wolfe,et al.  Guided Search 2.0 A revised model of visual search , 1994, Psychonomic bulletin & review.

[37]  W. Schultz Predictive reward signal of dopamine neurons. , 1998, Journal of neurophysiology.

[38]  Charles J. Wilson,et al.  Chapter II The basal ganglia , 1996 .

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

[40]  Shun-ichi Amari,et al.  Self-Organization in the Basal Ganglia with Modulation of Reinforcement Signals , 2002, Neural Computation.

[41]  Arvind Kumar,et al.  The High-Conductance State of Cortical Networks , 2008, Neural Computation.

[42]  O. Hikosaka,et al.  Eye movements in monkeys with local dopamine depletion in the caudate nucleus. II. Deficits in voluntary saccades , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  J. Wickens,et al.  Cellular models of reinforcement. , 1995 .

[44]  Joel L. Davis,et al.  Adaptive Critics and the Basal Ganglia , 1995 .

[45]  C. Gerfen,et al.  D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. , 1990, Science.

[46]  C. D. Stern,et al.  Handbook of Chemical Neuroanatomy Methods in Chemical Neuroanatomy. Edited by A. Bjorklund and T. Hokfelt. Elsevier, Amsterdam, 1983. Cloth bound, 548 pp. UK £140. (Volume 1 in the series). , 1986, Neurochemistry International.

[47]  H. Bergman,et al.  The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. , 1994, Journal of neurophysiology.

[48]  H. Kita,et al.  Dynorphin exerts both postsynaptic and presynaptic effects in the Globus pallidus of the rat. , 2000, Journal of neurophysiology.

[49]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  D. Heeger Normalization of cell responses in cat striate cortex , 1992, Visual Neuroscience.

[51]  V. Srinivasa Chakravarthy,et al.  What do the basal ganglia do? A modeling perspective , 2010, Biological Cybernetics.

[52]  J. Cohen,et al.  The role of locus coeruleus in the regulation of cognitive performance. , 1999, Science.

[53]  S. Amari Dynamics of pattern formation in lateral-inhibition type neural fields , 1977, Biological Cybernetics.

[54]  S. Grillner,et al.  Selection and initiation of motor behavior , 1997 .