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The primate amygdala represents the positive and negative value of visual stimuli during learning

Abstract

Visual stimuli can acquire positive or negative value through their association with rewards and punishments, a process called reinforcement learning. Although we now know a great deal about how the brain analyses visual information, we know little about how visual representations become linked with values. To study this process, we turned to the amygdala, a brain structure implicated in reinforcement learning1,2,3,4,5. We recorded the activity of individual amygdala neurons in monkeys while abstract images acquired either positive or negative value through conditioning. After monkeys had learned the initial associations, we reversed image value assignments. We examined neural responses in relation to these reversals in order to estimate the relative contribution to neural activity of the sensory properties of images and their conditioned values. Here we show that changes in the values of images modulate neural activity, and that this modulation occurs rapidly enough to account for, and correlates with, monkeys' learning. Furthermore, distinct populations of neurons encode the positive and negative values of visual stimuli. Behavioural and physiological responses to visual stimuli may therefore be based in part on the plastic representation of value provided by the amygdala.

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Figure 1: Task and brain MRI.
Figure 2: Behaviour and neural activity from a single amygdala neuron during learning.
Figure 3: Amygdala neurons encode the positive and negative value of visual stimuli.
Figure 4: The relationship between changes in neural activity and behavioural responses.

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Acknowledgements

We thank C. R. Gallistel for discussions and for assistance with the change-point test; S. Dashnaw and J. Hirsch for MRI support; C. A. Mason, E. R. Kandel, M. N. Shadlen and members of the Mahoney Center at Columbia for comments on the manuscript; and M. E. Goldberg, J. E. LeDoux and W. T. Newsome for mentoring during a career development award to C.D.S. This work was supported by the Keck foundation, grants from the NIMH, and the Klingenstein, Sloan and NARSAD foundations, and by a Charles E. Culpeper Scholarship award from Goldman Philanthropic Partnerships to C.D.S. J.J.P. received support from NICHD and NEI institutional training grants. S.E.M. received support from an NSF graduate research fellowship. Author Contributions J.J.P. and M.A.B. performed all experiments and conducted data analyses. S.E.M. performed some of the data analyses and contributed to many discussions. Experiments were designed and implemented in the laboratory of C.D.S.

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Correspondence to C. Daniel Salzman.

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The Supplementary Notes consists of Supplementary Figures 1–9 and their legends, Supplementary Notes 1–3, and Supplementary Methods. (PDF 643 kb)

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Paton, J., Belova, M., Morrison, S. et al. The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439, 865–870 (2006). https://doi.org/10.1038/nature04490

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