Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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


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.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.


  1. Maren, S. & Quirk, G. J. Neuronal signaling of fear memory. Nature Rev. Neurosci. 5, 844–852 (2004)

    CAS  Article  Google Scholar 

  2. LeDoux, J. E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155–184 (2000)

    CAS  Article  Google Scholar 

  3. Baxter, M. & Murray, E. A. The amygdala and reward. Nature Rev. Neurosci. 3, 563–573 (2002)

    CAS  Article  Google Scholar 

  4. Everitt, B. J., Cardinal, R. N., Parkinson, J. A. & Robbins, T. W. Appetitive behaviour: impact of amygdala-dependent mechanisms of emotional learning. Ann. NY Acad. Sci. 985, 233–250 (2003)

    ADS  Article  Google Scholar 

  5. Holland, P. C. & Gallagher, M. Amygdala circuitry in attentional and representational processes. Trends Cogn. Sci. 3, 65–73 (1999)

    CAS  Article  Google Scholar 

  6. Stefanacci, L. & Amaral, D. G. Some observations on cortical inputs to the macaque monkey amygdala: an anterograde tracing study. J. Comp. Neurol. 451, 301–323 (2002)

    Article  Google Scholar 

  7. Amaral, D., Price, J., Pitkanen, A. & Carmichael, S. in The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. Aggleton, J.) 1–66 (Wiley-Liss, New York, 1992)

    Google Scholar 

  8. McDonald, A. J. Cortical pathways to the mammalian amygdala. Prog. Neurobiol. 55, 257–332 (1998)

    CAS  Article  Google Scholar 

  9. Schultz, W., Dayan, P. & Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997)

    CAS  Article  Google Scholar 

  10. Ghashghaei, H. T. & Barbas, H. Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115, 1261–1279 (2002)

    CAS  Article  Google Scholar 

  11. Pavlov, I. P. Conditioned Reflexes (Oxford Univ. Press, London, 1927)

    Google Scholar 

  12. Gallistel, C. R., Fairhurst, S. & Balsam, P. The learning curve: implications of a quantitative analysis. Proc. Natl Acad. Sci. USA 101, 13124–13131 (2004)

    ADS  CAS  Article  Google Scholar 

  13. Green, D. M. & Swets, J. A. Signal Detection Theory and Psychophysics (John Wiley and Sons, New York, 1966)

    Google Scholar 

  14. Rolls, E. T., Critchley, H. D., Mason, R. & Wakeman, E. A. Orbitofrontal cortex neurons: role in olfactory and visual association learning. J. Neurophysiol. 75, 1970–1981 (1996)

    CAS  Article  Google Scholar 

  15. Wallis, J. D. & Miller, E. K. Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur. J. Neurosci. 18, 2069–2081 (2003)

    Article  Google Scholar 

  16. Roesch, M. R. & Olson, C. R. Neuronal activity related to reward value and motivation in primate frontal cortex. Science 304, 307–310 (2004)

    ADS  CAS  Article  Google Scholar 

  17. Tremblay, L. & Schultz, W. Relative reward preference in primate orbitofrontal cortex. Nature 398, 704–708 (1999)

    ADS  CAS  Article  Google Scholar 

  18. Saddoris, M. P., Gallagher, M. & Schoenbaum, G. Rapid associative encoding in basolateral amygdala depends on connections with orbitofrontal cortex. Neuron 46, 321–331 (2005)

    CAS  Article  Google Scholar 

  19. Schoenbaum, G., Setlow, B., Saddoris, M. P. & Gallagher, M. Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 39, 855–867 (2003)

    CAS  Article  Google Scholar 

  20. Schoenbaum, G., Chiba, A. & Gallagher, M. Orbitalfrontal cortex and basolateral amygdala encode expected outcomes during learning. Nature Neurosci. 1, 155–159 (1998)

    CAS  Article  Google Scholar 

  21. Freese, J. L. & Amaral, D. G. The organization of projections from the amygdala to visual cortical areas TE and V1 in the macque monkey. J. Comp. Neurol. 486, 295–317 (2005)

    Article  Google Scholar 

  22. Gottfried, J., O'Doherty, J. & Dolan, R. J. Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301, 1104–1107 (2003)

    ADS  CAS  Article  Google Scholar 

  23. LaBar, K. S., Gatenby, J. C., Gore, J. C., LeDoux, J. E. & Phelps, E. A. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20, 937–945 (1998)

    CAS  Article  Google Scholar 

  24. Sanghera, M. K., Rolls, E. T. & Roper-Hall, A. Visual responses of neurons in the dorsolateral amygdala of the alert monkey. Exp. Neurol. 63, 610–626 (1979)

    CAS  Article  Google Scholar 

  25. Rolls, E. in The Amygdala: A Functional Analysis (ed. Aggleton, J.) 447–478 (Oxford Univ. Press, New York, 2000)

    Google Scholar 

  26. Nishijo, H., Ono, T. & Nishino, H. Single neuron responses in amygdala of alert monkey during complex sensory stimulation with affective significance. J. Neurosci. 8, 3570–3583 (1988)

    CAS  Article  Google Scholar 

  27. Stefanacci, L., Suzuki, W. A. & Amaral, D. G. Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys. J. Comp. Neurol. 375, 552–582 (1996)

    CAS  Article  Google Scholar 

  28. Lee, H. J. et al. Role of amygdalo-nigral circuitry in conditioning of a visual stimulus paired with food. J. Neurosci. 25, 3881–3888 (2005)

    CAS  Article  Google Scholar 

  29. Fudge, J. L. & Haber, S. N. The central nucleus of the amygdala projection to dopamine subpopulations in primates. Neuroscience 97, 479–494 (2000)

    CAS  Article  Google Scholar 

  30. Davis, M. in The Amygdala: A Functional Analysis (ed. Aggleton, J.) 213–287 (Oxford Univ. Press, New York, 2000)

    Google Scholar 

Download references


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.

Author information

Authors and Affiliations


Corresponding author

Correspondence to C. Daniel Salzman.

Ethics declarations

Competing interests

Reprints and permissions information is available at The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

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

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing