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Selective and graded coding of reward uncertainty by neurons in the primate anterodorsal septal region

Nature Neuroscience volume 16, pages 756–762 (2013)Cite this article

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Abstract

Natural environments are uncertain. Uncertainty of emotional outcomes can induce anxiety and raise vigilance, promote and signal the opportunity for learning, modulate economic choice and regulate risk-seeking. Here we demonstrate that a subset of neurons in the anterodorsal region of the primate septum (ADS) are primarily devoted to processing uncertainty in a highly specific manner. Those neurons were selectively activated by visual cues indicating probabilistic delivery of reward (for example, 25%, 50% and 75% reward) and did not respond to cues indicating certain outcomes (0% and 100% reward). The average ADS uncertainty response was graded with the magnitude of reward uncertainty and selectively signaled uncertainty about rewards rather than punishments. The selective and graded information about reward uncertainty encoded by many neurons in the ADS may underlie modulation of uncertainty of value- and sensorimotor-related areas to regulate goal-directed behavior.

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Figure 1: Responses of reward-uncertainty neurons in the ADS to certain and uncertain predictions of rewards and punishment (experiment 1).
Figure 2: Locations of neurons tested for uncertainty coding.
Figure 3: Responses of reward-uncertainty neurons to information about reward uncertainty and reward amount (experiment 2).
Figure 4: Responses of reward-uncertainty neurons to uncertainty about different valued outcomes (experiment 3).
Figure 5: Responses of reward-uncertainty neurons during learning of novel conditioned stimuli (experiment 4).

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Acknowledgements

We thank E. Bromberg-Martin, B. Cumming, P. Daye, A. Ghazizadeh, S. Hong, H. Kim, D. Leopold, P. Rudebeck, K. Saleem, Y. Tachibana, R. Wurtz, S. Yamamoto and M. Yasuda for valuable scientific discussions, D. Leopold, F. Ye and C. Zhu for excellent MRI services and advice, M. Smith for histological expertise and service, and A. Hays, J. McClurkin, B. Nagy, N. Nichols, D. Parker and T. Ruffner for technical support. This work was supported by the intramural research program at the US National Eye Institute.

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Authors and Affiliations

  1. Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland, USA

    Ilya E Monosov & Okihide Hikosaka

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  1. Ilya E Monosov
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I.E.M. initiated the experiments, performed the experiments and analyzed the data in consultation with O.H.; I.E.M. and O.H. discussed the results and wrote the manuscript.

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Correspondence to Ilya E Monosov.

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Monosov, I., Hikosaka, O. Selective and graded coding of reward uncertainty by neurons in the primate anterodorsal septal region. Nat Neurosci 16, 756–762 (2013). https://doi.org/10.1038/nn.3398

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