Shaping of Motor Responses by Incentive Values through the Basal Ganglia

The striatum is a key neural interface for cognitive and motor information processing in which associations between reward value and visual stimulus can be used to modify motor commands. It can guide action–selection processes that occur farther downstream in the basal ganglia (BG) circuit, by encoding the reward value of an action. Here, we report on the study of simultaneously recorded neurons in the dorsal striatum (input stage of the BG) and the internal pallidum (output stage of the BG) in two monkeys performing a center-out motor task in which the visual targets were associated with different reward probabilities. We show that the tuning curves of motor-related neurons in both structures are modulated by the value of the action before movement initiation and during its execution. The representations of values associated with different actions change dynamically during the task in the internal globus pallidus, with a significant increase in the number of encoding neurons for the chosen target at the onset of movement. This report sheds additional light on the functional differences between the input and output structures of the BG and supports the assertion that the dorsal basal ganglia are involved in movement-related decision-making processes based on incentive values.

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

[2]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. , 1989, Journal of neurophysiology.

[4]  O. Hikosaka Models of information processing in the basal Ganglia edited by James C. Houk, Joel L. Davis and David G. Beiser, The MIT Press, 1995. $60.00 (400 pp) ISBN 0 262 08234 9 , 1995, Trends in Neurosciences.

[5]  A. Graybiel,et al.  Temporal and spatial characteristics of tonically active neurons of the primate's striatum. , 1995, Journal of neurophysiology.

[6]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[7]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[8]  M. E. Anderson,et al.  Pallidal discharge related to the kinematics of reaching movements in two dimensions. , 1997, Journal of neurophysiology.

[9]  J. Hollerman,et al.  Influence of reward expectation on behavior-related neuronal activity in primate striatum. , 1998, Journal of neurophysiology.

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

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

[12]  Wolfram Schultz,et al.  Behavioral reactions reflecting differential reward expectations in monkeys , 2001, Experimental Brain Research.

[13]  J. Wickens,et al.  A cellular mechanism of reward-related learning , 2001, Nature.

[14]  D Guilloteau,et al.  Pallidal border cells: an anatomical and electrophysiological study in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated monkey , 2001, Neuroscience.

[15]  B Bioulac,et al.  Dopamine agonist-induced dyskinesias are correlated to both firing pattern and frequency alterations of pallidal neurones in the MPTP-treated monkey. , 2001, Brain : a journal of neurology.

[16]  O. Hikosaka,et al.  Correlation of primate caudate neural activity and saccade parameters in reward-oriented behavior. , 2003, Journal of neurophysiology.

[17]  W. Schultz,et al.  Discrete Coding of Reward Probability and Uncertainty by Dopamine Neurons , 2003, Science.

[18]  Tatsuo K Sato,et al.  Correlated Coding of Motivation and Outcome of Decision by Dopamine Neurons , 2003, The Journal of Neuroscience.

[19]  O. Hikosaka,et al.  Reward-predicting activity of dopamine and caudate neurons--a possible mechanism of motivational control of saccadic eye movement. , 2004, Journal of neurophysiology.

[20]  E. Vaadia,et al.  Independent Coding of Movement Direction and Reward Prediction by Single Pallidal Neurons , 2004, The Journal of Neuroscience.

[21]  E. Vaadia,et al.  Coincident but Distinct Messages of Midbrain Dopamine and Striatal Tonically Active Neurons , 2004, Neuron.

[22]  K. Doya,et al.  Representation of Action-Specific Reward Values in the Striatum , 2005, Science.

[23]  W. Schultz,et al.  Adaptive Coding of Reward Value by Dopamine Neurons , 2005, Science.

[24]  C. Bruce,et al.  Neural circuitry of judgment and decision mechanisms , 2005, Brain Research Reviews.

[25]  P. Glimcher,et al.  Midbrain Dopamine Neurons Encode a Quantitative Reward Prediction Error Signal , 2005, Neuron.

[26]  Wolfram Schultz,et al.  Relative reward processing in primate striatum , 2005, Experimental Brain Research.

[27]  D. Hansel,et al.  Competition between Feedback Loops Underlies Normal and Pathological Dynamics in the Basal Ganglia , 2022 .

[28]  E. Vaadia,et al.  Midbrain dopamine neurons encode decisions for future action , 2006, Nature Neuroscience.

[29]  W. Schultz Behavioral theories and the neurophysiology of reward. , 2006, Annual review of psychology.