Skip to main content

Thank you for visiting nature.com. 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.

Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning

Nature Neuroscience volume 1, pages 155–159 (1998)Cite this article

Abstract

Reciprocal connections between the orbitofrontal cortex and the basolateral nucleus of the amygdala may provide a critical circuit for the learning that underlies goal-directed behavior. We examined neural activity in rat orbitofrontal cortex and basolateral amygdala during instrumental learning in an olfactory discrimination task. Neurons in both regions fired selectively during the anticipation of rewarding or aversive outcomes. This selective activity emerged early in training, before the rats had learned reliably to avoid the aversive outcome. The results support the concept that the basolateral amygdala and orbitofrontal cortex cooperate to encode information that may be used to guide goal-directed behavior.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Photomicrographs of histological sections showing the reconstruction of recording sites in representative subjects in (a) OFC and (b) ABL.
Figure 2: Sequence of behaviors in (a) positive go, (b) negative go, and (c) negative no-go trials during acquisition of a go, no-go olfactory discrimination task.
Figure 3: Differential activity during the delay following a go response on pre-criterion trials in a neuron recorded in OFC and a neuron recorded in ABL during two-odor discrimination training.
Figure 4: Contrast in activity on positive and negative go trials during the early (open bars) and late (closed bars) segments of pre-criterion training for a population of neurons selective during the delay in OFC and ABL (see Methods for description of early and late segments and criteria for the analysis).
Figure 5: Activity of the OFC neuron in Fig. 3 on positive go, negative go, and negative no-go trials.

References

  1. Fuster, J.M. in Cerebral Cortex (eds Jones, E.G. & Peters, A.) 151– 177 (Plenum, New York, 1985)

    Google Scholar 

  2. Goldman-Rakic, P.S. The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. Phil. Trans. R. Soc. Lond. 351, 1445–1453 ( 1996)

    Article  CAS  Google Scholar 

  3. Petrides, M. Specialized systems for the processing of mnemonic information within the primate prefrontal cortex. Phil. Trans. R. Soc. Lond. 351, 1455–1462 (1996)

    Article  CAS  Google Scholar 

  4. Damasio, A R. Decartes Error. (G.P. Putnam, New York, 1994)

    Google Scholar 

  5. Rolls, E.T. The orbitofrontal cortex. Phil. Trans. R. Soc. Lond. 351, 1433–1443 (1996)

    Article  CAS  Google Scholar 

  6. Bechara, A., Damasio, H., Tranel, D. & Damasio, A.R. Deciding advantageously before knowing the advantageous strategy. Science 275 , 1293–1294 (1997)

    Article  CAS  Google Scholar 

  7. Bechara, A., Damasio, H., Tranel, D. & Damasio, A.R. Dissociation of working memory from decision making within the human prefrontal cortex . J. Neurosci. 18, 428– 437 (1998)

    Article  CAS  Google Scholar 

  8. Krettek, J.E. & Price, J.L. Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat. J. Comp. Neurol. 172, 687–722 (1977)

    Article  CAS  Google Scholar 

  9. Kolb, B. Functions of the frontal cortex of the rat: A comparative review. Brain Res. Rev. 8, 65–98 (1984 )

    Article  Google Scholar 

  10. Price, J.L., Russchen, F.T. & Amaral, D.G. in Integrated Systems of the CNS, Part I. Handbook of Chemical Neuroanatomy, Vol. 5 (eds Bjorklund, A. Hokfelt, T. & Swanson, L.W.) 279–388 (Elsevier, Amsterdam, 1987)

    Google Scholar 

  11. McDonald, A.J. Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 44, 1– 44 (1991)

    Article  CAS  Google Scholar 

  12. Gallagher, M. & Chiba, A.A. The amygdala and emotion. Curr. Opinion Neurobiol. 6, 221–227 (1996)

    Article  CAS  Google Scholar 

  13. Killcross, S., Robbins, T.W. & Everitt, B.J. Different types of fear-conditioned behavior mediated by separate nuclei within amygdala. Nature 388, 377–380 (1997)

    Article  CAS  Google Scholar 

  14. Malkova, L., Gaffan, D. & Murray, E.A. Excitotoxic lesions of the amygdala fail to produce impairment in visual learning for auditory secondary reinforcement but interfere with reinforcer devaluation effects in rhesus monkeys. J. Neurosci. 17, 6011–6020 (1997)

    Article  CAS  Google Scholar 

  15. Hatfield, T., Han, J.-S., Conley, M., Gallagher, M. & Holland, P. Neurotoxic lesions of basolateral, but not central, amygdala interfere with pavlovian second-order conditioning and reinforcer devaluation effects. J. Neurosci. 16, 5256 –5265 (1996)

    Article  CAS  Google Scholar 

  16. Balleine, B.W., Leibeskind, J.C. & Dickinson, A. Effect of cell body lesions of the basolateral amygdala on instrumental conditioning. Soc. Neurosci. Abstr. 23, 786 (1997)

    Google Scholar 

  17. Jones, B. & Mishkin, M. Limbic lesions and the problem of stimulus-reinforcement associations. Exp. Neurol. 36 , 362–377 (1972)

    Article  CAS  Google Scholar 

  18. Kling, A., Steklis, H.D. & Deutsch, S.D. in The Neurobiology of the Amygdala (ed Eleftheriou, B.E.) 611–632 (Plenum, New York, 1972)

    Google Scholar 

  19. Brown, S. & Schaefer, E.A. An investigation into the function of the occipital and temporal lobe of the monkey's brain. Phil. Trans. R. Soc. Lond. 179, 303 ( 1888)

    Google Scholar 

  20. Kluver, H. & Bucy, P.C. Preliminary analysis of functions of the temporal lobes in monkeys. Arch. Neurol. Psychiatry 42, 979–1000 (1939)

    Article  Google Scholar 

  21. Kolb, B. in The Cerebral Cortex of the Rat (eds Kolb, B. & Tees, R.C.) 437– 458 (MIT Press, Cambridge, Massachusetts, 1990)

    Google Scholar 

  22. Schoenbaum, G. & Eichenbaum, H. Information coding in the rodent prefrontal cortex. I. Single neuron activity in orbitofrontal cortex compared with that in piriform cortex. J. Neurophysiol. 74, 733–750 (1995)

    Article  CAS  Google Scholar 

  23. Schoenbaum, G. & Eichenbaum, H. Information coding in the rodent prefrontal cortex. II. Ensemble activity in orbitofrontal cortex. J. Neurophysiol. 74, 751–762 (1995)

    Article  CAS  Google Scholar 

  24. Critchley, H.D. & Rolls, E.T. Olfactory neuronal responses in the primate orbitofrontal cortex: analysis in an olfactory discrimination task. J. Neurophysiol. 75, 1659– 1672 (1996)

    Article  CAS  Google Scholar 

  25. Fuster, J.M. Unit activity in the prefrontal cortex during delayed response performance: Neuronal correlates of short-term memory. J. Neurophysiol. 36, 61–78 (1973)

    Article  CAS  Google Scholar 

  26. Niki, H. Differential activity of prefrontal units during right and left delayed response trials. Brain Res. 70, 346–349 ( 1974)

    Article  CAS  Google Scholar 

  27. Funahashi, S., Bruce, C.J. & Goldman-Rakic, P.S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J. Neurophysiol. 61, 331–349 (1989)

    Article  CAS  Google Scholar 

  28. Miller, E.K., Erickson, C.A. & Desimone, R. Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J. Neurosci. 16, 5154–5167 (1996)

    Article  CAS  Google Scholar 

  29. Fuster, J.M., Bauer, R.H. & Jervey, J.P. Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks. Exp. Neurol. 77, 679–694 (1982)

    Article  CAS  Google Scholar 

  30. Watanabe, M. Reward expectancy in primate prefrontal neurons. Nature 382, 629–632 (1996)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank T. Lam for assistance in figure preparation, Dr. M. Burchinal and E. Neebe for statistical consultation. This work was supported by funding from the NIH.

Author information

Authors and Affiliations

  1. Department of Psychology, Johns Hopkins University, 3400 North Charles St, 25 Ames Hall, Baltimore, 21218, Maryland, USA

    Geoffrey Schoenbaum & Michela Gallagher

  2. Cognitive Science Department, University of California at San Diego, 9500 Gilman Drive - 0515, La Jolla, 92093, California, USA

    Andrea A. Chiba

Authors
  1. Geoffrey Schoenbaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea A. Chiba
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michela Gallagher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Geoffrey Schoenbaum.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Schoenbaum, G., Chiba, A. & Gallagher, M. Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nat Neurosci 1, 155–159 (1998). https://doi.org/10.1038/407

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/407

This article is cited by

Search

Advanced search

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