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Lateral habenula neurons signal errors in the prediction of reward information

An Erratum to this article was published on 23 November 2011

This article has been updated

Abstract

Humans and animals have the ability to predict future events, which they cultivate by continuously searching their environment for sources of predictive information. However, little is known about the neural systems that motivate this behavior. We hypothesized that information-seeking is assigned value by the same circuits that support reward-seeking, such that neural signals encoding reward prediction errors (RPEs) include analogous information prediction errors (IPEs). To test this, we recorded from neurons in the lateral habenula, a nucleus that encodes RPEs, while monkeys chose between cues that provided different chances to view information about upcoming rewards. We found that a subpopulation of lateral habenula neurons transmitted signals resembling IPEs, responding when reward information was unexpectedly cued, delivered or denied. These signals evaluated information sources reliably, even when the monkey's decisions did not. These neurons could provide a common instructive signal for reward-seeking and information-seeking behavior.

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Figure 1: Behavioral preference to view informative reward cues.
Figure 2: Lateral habenula neurons transmit an inverted RPE signal.
Figure 3: Lateral habenula activity related to IPEs evoked by the information-predictive targets.
Figure 4: Information-related signals are strongest in a subpopulation of neurons.
Figure 5: Lateral habenula activity related to negative IPEs evoked by denial of reward information.
Figure 6: Lateral habenula activity related to positive IPEs evoked by delivery of reward information.
Figure 7: Joint coding of IPEs and cRPEs in single neurons.
Figure 8: Lateral habenula and dopamine neurons signal information probability reliably despite variable decisions.

Change history

  • 22 September 2011

    In the version of this article initially published, the colored circles and horizontal bars above the x axis in the top panels of Figure 8, which indicate the median and central 90% range of each distribution, were misaligned. The error has been corrected in the HTML and PDF versions of the article.

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Acknowledgements

We thank M. Matsumoto, S. Hong, I. Monosov, M. Yasuda, S. Yamamoto, Y. Tachibana, H. Kim and D. Lee for valuable discussions. This work was supported by the intramural research program at the National Eye Institute.

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E.S.B.-M. designed and performed the experiments and analyzed the data. O.H. supported these processes. E.S.B.-M. and O.H. discussed the results and wrote the manuscript.

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Correspondence to Ethan S Bromberg-Martin.

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Bromberg-Martin, E., Hikosaka, O. Lateral habenula neurons signal errors in the prediction of reward information. Nat Neurosci 14, 1209–1216 (2011). https://doi.org/10.1038/nn.2902

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