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The amygdala and reward

Nature Reviews Neuroscience volume 3, pages 563–573 (2002)Cite this article

Key Points

  • It is widely accepted that the amygdala is associated with fear conditioning and the processing of negative emotions. But this structure is also involved in the processing of positive emotions, and particularly in learning about the positive value of stimuli.

  • A number of types of behaviour that involve reward processing are independent of the amygdala. These include visual-discrimination learning, visuomotor conditional learning, food-cup approach (Pavlovian conditioning), and food and object preferences.

  • These behaviours, in the absence of stimulus–reward association mediated by the amygdala, could rely on stimulus–response learning or cortical representations of the value of stimuli.

  • Different divisions of the amygdala mediate different kinds of stimulus–value association. Lesions of the basolateral nucleus of the amygdala impair performance on tasks that require linking an object with a current (as opposed to a consistent) stimulus value. Examples of paradigms that can expose this effect include reinforcer devaluation (in which the value of a reinforcer changes) and second-order conditioning (in which a previously neutral stimulus comes to acquire the value of the reinforcer with which it has been paired).

  • Neurons of the basolateral amygdala, like neurons in the prefrontal cortex, show complex patterns of firing that include specific responses to particular objects, such as foods. These patterns of firing can be modulated by reinforcer devaluation.

  • Lesions of the central nucleus of the amygdala, by contrast, impair Pavlovian approach or avoidance responses to specific conditioned stimuli. An example of Pavlovian approach is the increased rearing response of rats to a light that is repeatedly paired with food delivery.

  • Patients with bilateral amygdala damage perform poorly on laboratory-based gambling tasks. Unlike patients with damage to the prefrontal cortex, who are also impaired on these tasks, patients with amygdala damage fail to generate normal changes in skin-conductance response and other autonomic responses when they 'win' or 'lose' money. Their inability to learn a winning strategy might result from an inability to generate the appropriate affective state.

  • Future work should aim to integrate these functions of the amygdala with its other functions, such as the production of fear responses and attentional processing.

Abstract

The amygdala — an almond-shaped group of nuclei at the heart of the telencephalon — has been associated with a range of cognitive functions, including emotion, learning, memory, attention and perception. Most current views of amygdala function emphasize its role in negative emotions, such as fear, and in linking negative emotions with other aspects of cognition, such as learning and memory. However, recent evidence supports a role for the amygdala in processing positive emotions as well as negative ones, including learning about the beneficial biological value of stimuli. Indeed, the amygdala's role in stimulus–reward learning might be just as important as its role in processing negative affect and fear conditioning.

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Figure 1: Anatomical relationships of the basolateral complex and the central nucleus of the amygdala in macaque monkeys.
Figure 2: Reinforcer-devaluation task.
Figure 3: Second-order conditioning.
Figure 4: Neuronal firing in the basolateral amygdala and the orbital frontal cortex during the delay portion of trials in a two-odour discrimination task.

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Acknowledgements

The authors would like to thank S. P. Wise for helpful comments on an earlier version of the paper. M.G.B. is an Alfred P. Sloan Research Fellow. The research of E.A.M is supported by the Intramural Research Program of the National Institutes of Mental Health.

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Authors and Affiliations

  1. Department of Psychology, Harvard University, 906 William James Hall, 33 Kirkland Street, Cambridge, 02138, Massachusetts, USA

    Mark G. Baxter

  2. Laboratory of Neuropsychology, National Institute of Mental Health, 49 Convent Drive, Building 49, Room 1B80, Bethesda, 20892-4415, Maryland, USA

    Elisabeth A. Murray

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FURTHER INFORMATION

Elisabeth Murray's lab

Mark Baxter's lab

Encyclopedia of Life Sciences

learning and memory

MIT Encyclopedia of Cognitive Sciences

amygdala, primate

conditioning and the brain

magnetic resonance imaging

Glossary

EXCITOTOXIN

A chemical toxin — typically a structural analogue of the neurotransmitter glutamate — that, when injected into brain tissue, kills cell bodies in the region of injection, leaving fibres of passage through that region intact. The neurotoxic effect of these agents is mediated by their action at glutamate receptors and involves overstimulation of the neuron, which leads to cell death.

DELAYED NONMATCHING-TO-SAMPLE

A test of stimulus-recognition memory in which the subject is presented with one or more sample objects and, after a short delay, is confronted with a choice test between the sample object and a novel object. The subject is rewarded for choosing the novel object.

INSTRUMENTAL LEARNING

Learning that takes place through reinforcement (or the absence of punishment) that is contingent on the performance (or withholding) of a particular behaviour. So, the subject's response is instrumental in producing an outcome, typically a food reward. Compare with Pavlovian learning.

PAVLOVIAN LEARNING

Learning that takes place because of temporal contiguity between a stimulus (the conditioned stimulus) and a reinforcer (the unconditioned stimulus), in the absence of a requirement for the subject to produce a particular behaviour to obtain reinforcement. Also commonly referred to as classical conditioning.

CROSSED-DISCONNECTION LESION

This involves crossed unilateral lesions of two neural structures, one in each hemisphere of the brain. Because each hemisphere has one of the two structures intact, communication between the two structures is selectively disrupted. This procedure is commonly carried out to determine whether two brain structures functionally interact in a particular behaviour.

VENTROMEDIAL PREFRONTAL CORTEX

The regions of the cerebral cortex on the ventral and medial surfaces of the frontal lobes, including the orbital frontal cortex, the gyrus rectus and the anterior cingulate cortex. 'Orbital frontal' or 'orbital prefrontal' cortex usually refers more specifically to the cortex on the orbital surface of the frontal lobe, including Walker's areas 10, 11, 13 and 14.

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Baxter, M., Murray, E. The amygdala and reward. Nat Rev Neurosci 3, 563–573 (2002). https://doi.org/10.1038/nrn875

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