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Representation of negative motivational value in the primate lateral habenula

Nature Neuroscience volume 12, pages 77–84 (2009)Cite this article

Abstract

An action may lead to either a reward or a punishment. Therefore, an appropriate action needs to be chosen on the basis of the values of both expected rewards and expected punishments. To understand the underlying neural mechanisms, we conditioned monkeys using a Pavlovian procedure with two distinct contexts: one in which rewards were available and another in which punishments were feared. We found that the population of lateral habenula neurons was most strongly excited by a conditioned stimulus associated with the most unpleasant event in each context: the absence of the reward or the presence of the punishment. The population of lateral habenula neurons was also excited by the punishment itself and inhibited by the reward itself, especially when they were less predictable. These results suggest that the lateral habenula has the potential to adaptively control both reward-seeking and punishment-avoidance behaviors, presumably through its projections to dopaminergic and serotonergic systems.

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Figure 1: Pavlovian procedure with two distinct contexts.
Figure 2: Responses of lateral habenula neurons to conditioned stimuli.
Figure 3: Relationship between objective value and conditioned stimulus response.
Figure 4: Changes in the averaged responses of the 49 neurons to 0% reward conditioned stimulus (black) and 0% airpuff conditioned stimulus (gray) after the block context was reversed.
Figure 5: Responses of lateral habenula neurons to unconditioned stimuli.
Figure 6: Responses of lateral habenula neurons to unconditioned stimulus omission.
Figure 7: Relationship between prediction error and unconditioned stimulus response.
Figure 8: Comparison between conditioned stimulus response and unconditioned stimulus response.

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Acknowledgements

We thank S. Hong, M. Yasuda and E. Bromberg-Martin for valuable discussion, and M.K. Smith, J.W. McClurkin, A.M. Nichols, T.W. Ruffner, A.V. Hays and L.P. Jensen for technical assistance. This research was supported by the Intramural Research Program at the National Institutes of Health, National Eye Institute.

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Authors and Affiliations

  1. Laboratory of Sensorimotor Research, National Eye Institute, US National Institutes of Health, 49 Convent Drive, Bethesda, 20892-4435, Maryland, USA

    Masayuki Matsumoto & Okihide Hikosaka

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  1. Masayuki Matsumoto
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Contributions

M.M. designed the Pavlovian procedure, performed the experiments and analyzed the data. O.H. supported all of these processes. M.M. and O.H. discussed the results and wrote the manuscript.

Corresponding author

Correspondence to Masayuki Matsumoto.

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Matsumoto, M., Hikosaka, O. Representation of negative motivational value in the primate lateral habenula. Nat Neurosci 12, 77–84 (2009). https://doi.org/10.1038/nn.2233

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