A neural correlate of response bias in monkey caudate nucleus

Primates are equipped with neural circuits in the prefrontal cortex, the parietal cortex and the basal ganglia that predict the availability of reward during the performance of behavioural tasks. It is not known, however, how reward value is incorporated in the control of action. Here we identify neurons in the monkey caudate nucleus that create a spatially selective response bias depending on the expected gain. In behavioural tasks, the monkey had to make a visually guided eye movement in every trial, but was rewarded for a correct response in only half of the trials. Reward availability was predictable on the basis of the spatial position of the visual target. We found that caudate neurons change their discharge rate systematically, even before the appearance of the visual target, and usually fire more when the contralateral position is associated with reward. Strong anticipatory activity of neurons with a contralateral preference is associated with decreased latency for eye movements in the contralateral direction. We conclude that this neuronal mechanism creates an advance bias that favours a spatial response when it is associated with a high reward value.

[1]  D. Bindra Neuropsychological interpretation of the effects of drive and incentive-motivation on general activity and instrumental behavior. , 1968 .

[2]  W. F. Prokasy,et al.  Classical conditioning II: Current research and theory. , 1972 .

[3]  S. Thorpe,et al.  Responses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus , 1983, Behavioural Brain Research.

[4]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. , 1983, Journal of neurophysiology.

[5]  M. Levine,et al.  The GABAergic striatonigral neurons of the cat: demonstration by double peroxidase labeling , 1986, Brain Research.

[6]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. , 1989, Journal of neurophysiology.

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

[8]  C. Wilson,et al.  Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  W. Schultz,et al.  Neuronal activity in monkey ventral striatum related to the expectation of reward , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  W. Schultz,et al.  Neuronal activity in monkey striatum related to the expectation of predictable environmental events. , 1992, Journal of neurophysiology.

[11]  B. Balleine,et al.  Motivational control of goal-directed action , 1994 .

[12]  Masataka Watanabe Reward expectancy in primate prefrental neurons , 1996, Nature.

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

[14]  Michele A. Basso,et al.  Modulation of neuronal activity by target uncertainty , 1997, Nature.

[15]  E. Rolls The Brain and Emotion , 2000 .

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

[17]  D. Munoz,et al.  Saccadic Probability Influences Motor Preparation Signals and Time to Saccadic Initiation , 1998, The Journal of Neuroscience.

[18]  M. Shadlen,et al.  Effect of Expected Reward Magnitude on the Response of Neurons in the Dorsolateral Prefrontal Cortex of the Macaque , 1999, Neuron.

[19]  Michael L. Platt,et al.  Neural correlates of decision variables in parietal cortex , 1999, Nature.

[20]  W. Schultz,et al.  Relative reward preference in primate orbitofrontal cortex , 1999, Nature.

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

[22]  J Schlag,et al.  Reward-predicting and reward-detecting neuronal activity in the primate supplementary eye field. , 2000, Journal of neurophysiology.

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

[24]  Okihide Hikosaka,et al.  Role of Primate Substantia Nigra Pars Reticulata in Reward-Oriented Saccadic Eye Movement , 2002, The Journal of Neuroscience.

[25]  O. Hikosaka,et al.  Influence of reward expectation on visuospatial processing in macaque lateral prefrontal cortex. , 2002, Journal of neurophysiology.

[26]  O. Hikosaka,et al.  Feature-Based Anticipation of Cues that Predict Reward in Monkey Caudate Nucleus , 2002, Neuron.

[27]  O. Hikosaka,et al.  Reward-dependent spatial selectivity of anticipatory activity in monkey caudate neurons. , 2002, Journal of neurophysiology.