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J Neurophysiol 95: 567-584, 2006; doi:10.1152/jn.00458.2005
0022-3077/06 $8.00
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REVIEW

Basal Ganglia Orient Eyes to Reward

Okihide Hikosaka1, Kae Nakamura1 and Hiroyuki Nakahara2

1Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland; and 2Laboratory for Mathematical Neuroscience, RIKEN Brain Science Institute, Saitama, Japan

Submitted 4 April 2005; accepted in final form 23 September 2005

ABSTRACT

Expectation of reward motivates our behaviors and influences our decisions. Indeed, neuronal activity in many brain areas is modulated by expected reward. However, it is still unclear where and how the reward-dependent modulation of neuronal activity occurs and how the reward-modulated signal is transformed into motor outputs. Recent studies suggest an important role of the basal ganglia. Sensorimotor/cognitive activities of neurons in the basal ganglia are strongly modulated by expected reward. Through their abundant outputs to the brain stem motor areas and the thalamocortical circuits, the basal ganglia appear capable of producing body movements based on expected reward. A good behavioral measure to test this hypothesis is saccadic eye movement because its brain stem mechanism has been extensively studied. Studies from our laboratory suggest that the basal ganglia play a key role in guiding the gaze to the location where reward is available. Neurons in the caudate nucleus and the substantia nigra pars reticulata are extremely sensitive to the positional difference in expected reward, which leads to a bias in excitability between the superior colliculi such that the saccade to the to-be-rewarded position occurs more quickly. It is suggested that the reward modulation occurs in the caudate where cortical inputs carrying spatial signals and dopaminergic inputs carrying reward-related signals are integrated. These data support a specific form of reinforcement learning theories, but also suggest further refinement of the theory.

Address for reprint requests and other correspondence: O. Hikosaka, Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, MD 20892 (E-mail: oh{at}lsr.nei.nih.gov)




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