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Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala

Abstract

The amygdala has long been thought to be involved in emotional behaviour1,2, and its role in anxiety and conditioned fear has been highlighted3,4. Individual amygdaloid nuclei have been shown to project to various cortical and subcortical regions implicated in affective processing5,6,7. Here we show that some of these nuclei have separate roles in distinct mechanisms underlying conditioned fear responses. Rats with lesions of the central nucleus exhibited reduction in the suppression of behaviour elicited by a conditioned fear stimulus, but were simultaneously able to direct their actions to avoid further presentations of this aversive stimulus. In contrast, animals with lesions of the basolateral amygdala were unable to avoid the conditioned aversive stimulus by their choice behaviour, but exhibited normal conditioned suppression to this stimulus. This double dissociation demonstrates that distinct neural systems involving separate amygdaloid nuclei mediate different types of conditioned fear behaviour. We suggest that theories of amygdala function should take into account the roles of discrete amygdala subsystems in controlling different components of integrated emotional responses.

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Figure 1: Left, Difference between suppression ratios during presentation of the aversive CS+ and neutral CS− in sham-operated control rats, and animals with lesions of the lateral/basolateral nuclei of the amygdala (blA), the nucleus (cnA), or with combined lesions of both (cnA + blA)) averaged over 10 sessions.
Figure 2: Representation of largest (pale shading) and smallest (dark shading) lesions of: a, lateral/basolateral nuclei; b, central nucleus; and c, both basolateral and central nuclei of the amygdala.
Figure 3: Photomicrographs of sections from three representative brains showing an intact brain (a, b) and excitotoxic lesions of the basolateral (c, d) and central (e,f) amygdala. a, b, A section (right side) through the amygdala of a sham-operated control at low (a) and higher (b) magnification.

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Acknowledgements

We thank C. Morrison and H. Sweet for help with histology. This work was supported by a grant from the Human Frontiers Science Program, and a research fellowship to S.K. from Magdalene College, Cambridge.

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Correspondence to Simon Killcross.

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Killcross, S., Robbins, T. & Everitt, B. Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature 388, 377–380 (1997). https://doi.org/10.1038/41097

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