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The Journal of Neuroscience, May 14, 2008, 28(20):5331-5343; doi:10.1523/JNEUROSCI.0021-08.2008

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Behavioral/Systems/Cognitive
Reward-Dependent Modulation of Neuronal Activity in the Primate Dorsal Raphe Nucleus

Kae Nakamura, Masayuki Matsumoto, and Okihide Hikosaka

Laboratory of Sensorimotor Research, National Eye Institute–National Institutes of Health, Bethesda, Maryland 20892-4435

Correspondence should be addressed to Kae Nakamura at her present address: Department of Physiology, Kansai Medical University, School of Medicine, 10-15, Fumizono-cho, Moriguchi-city, Osaka 570-8506, Japan. Email: nakamkae{at}takii.kmu.ac.jp

The dopamine system has been thought to play a central role in guiding behavior based on rewards. Recent pharmacological studies suggest that another monoamine neurotransmitter, serotonin, is also involved in reward processing. To elucidate the functional relationship between serotonin neurons and dopamine neurons, we performed single-unit recording in the dorsal raphe nucleus (DRN), a major source of serotonin, and the substantia nigra pars compacta, a major source of dopamine, while monkeys performed saccade tasks in which the position of the target indicated the size of an upcoming reward. After target onset, but before reward delivery, the activity of many DRN neurons was modulated tonically by the expected reward size with either large- or small-reward preference, whereas putative dopamine neurons had phasic responses and only preferred large rewards. After reward delivery, the activity of DRN neurons was modulated tonically by the received reward size with either large- or small-reward preference, whereas the activity of dopamine neurons was not modulated except after the unexpected reversal of the position–reward contingency. Thus, DRN neurons encode the expected and received rewards, whereas dopamine neurons encode the difference between the expected and received rewards. These results suggest that the DRN, probably including serotonin neurons, signals the reward value associated with the current behavior.

Key words: serotonin; dopamine; raphe; saccade; primate; reinforcement; reward

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Received Jan. 3, 2008; revised April 7, 2008; accepted April 8, 2008.

Correspondence should be addressed to Kae Nakamura at her present address: Department of Physiology, Kansai Medical University, School of Medicine, 10-15, Fumizono-cho, Moriguchi-city, Osaka 570-8506, Japan. Email: nakamkae{at}takii.kmu.ac.jp

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