Roles of the Lateral Habenula and Anterior Cingulate Cortex in Negative Outcome Monitoring and Behavioral Adjustment in Nonhuman Primates.
Animals monitor the outcome of their choice and adjust subsequent choice behavior using the outcome information. Together with the anterior cingulate cortex (ACC), the lateral habenula (LHb) has recently attracted attention for its crucial role in monitoring negative outcome. To investigate their contributions to subsequent behavioral adjustment, we recorded single-unit activity from the LHb and ACC in monkeys performing a reversal learning task. The monkey was required to shift a previous choice to the alternative if the choice had been repeatedly unrewarded in past trials. We found that ACC neurons stored outcome information from several past trials, whereas LHb neurons detected the ongoing negative outcome with shorter latencies. ACC neurons, but not LHb neurons, signaled a behavioral shift in the next trial. Our findings suggest that, although both the LHb and the ACC represent signals associated with negative outcome, these structures contribute to subsequent behavioral adjustment in different ways.
Systems Neuroscience Section, Department of Cellular and Molecular Biology, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan; Department of Psychological Science, Kwansei Gakuin University, Nishinomiya, Hyogo 662-8501, Japan; Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8577, Japan; The Japan Society for the Promotion of Science, Chiyoda-ku, Tokyo 102-0083, Japan.
Takashi
T
Kawai
Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8577, Japan; Division of Biomedical Science, Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki 305-8577, Japan.
Hiroshi
H
Yamada
Department of Psychological Science, Kwansei Gakuin University, Nishinomiya, Hyogo 662-8501, Japan.
Nobuya
N
Sato
Systems Neuroscience Section, Department of Cellular and Molecular Biology, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Masahiko
M
Takada
Systems Neuroscience Section, Department of Cellular and Molecular Biology, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan; Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8577, Japan; Division of Biomedical Science, Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki 305-8577, Japan. Electronic address: mmatsumoto@md.tsukuba.ac.jp.
Masayuki
M
Matsumoto
D000223:Adaptation, Psychological / Q000502:physiology; D000818:Animals; D001522:Behavior, Animal / Q000502:physiology*; D001921:Brain / Q000166:cytology / Q000502:physiology; D001931:Brain Mapping; D002755:Choice Behavior / Q000502:physiology*; D006179:Gyrus Cinguli / Q000166:cytology / Q000502:physiology*; D019262:Habenula / Q000166:cytology / Q000502:physiology*; D008251:Macaca; D008253:Macaca mulatta; D008297:Male; D009474:Neurons / Q000502:physiology*; D012193:Reversal Learning / Q000502:physiology*