Review
The amygdala and appraisal processes: stimulus and response complexity as an organizing factor

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Abstract

The amygdala has been implicated in a variety of functions, ranging from attention to memory to emotion. In theories about the amygdala's role in conditioned fear, the lateral amygdala (LA) is the primary, perhaps unique, interface for incoming conditioned sensory stimuli and the central nucleus is the major output station. Recent studies indicate, however, that amygdala output pathways may be dissociated as a function of the type of conditioned fear behavior. Based on behavioral, electrophysiological and anatomical evidence, the present discussion proposes a modification of the traditional model of input pathways to the amygdala such that the LA activation as a sensory interface is limited to relatively simple, unimodal conditioned stimulus features whereas the basal amygdaloid nucleus (B) may serve as an amygdaloid sensory interface for complex, configural conditioned stimulus information. We further argue that the partition of amygdalar nuclei according to a complexity dimension appears to correspond both for input and output pathways and thus constitutes a common organizing factor in the functional anatomy of the amygdala. The extensive intra-amygdala wiring is assumed to underlie the computations necessary to perform behavioral decisions of various levels of complexity. Collectively, these results endow the amygdala with a more sophisticated role in guiding motivation and behavior.

Section snippets

Background: the intrices of Pavlovian fear conditioning

Pavlovian conditioning has a long and illustrious history, starting from its namesake and continuing today [44]. Based on the immense literature addressing the behavioral characteristics of Pavlovian conditioning, it is the paradigm of choice for research on the neurobiology of learning and memory, and it constitutes the general methodological framework of the present review.

One form of Pavlovian conditioning that has received considerable attention in neuroscientific studies over the last

The amygdala and fear conditioning: the significance of circuitry

Since the discovery that lesions of the amygdala produce altered social responses in a variety of conditions [25], a role has been ascribed for the amygdala in associating stimuli with specific outcomes, such as an impending fearful situation. It is well embedded within contemporary views of emotional learning that the amygdala plays a pivotal role in the formation and consolidation of aversive memories formed during fear conditioning [9], [27], [38].

The amygdala is a multinuclear complex.

The complexity dimension as an organizing factor of amygdala circuitry: a hypothesis

Given that the processing of a tone may be considered simple because of its unimodal and discrete nature, whereas the processing of a background context may be more complex because it is multimodal and temporally diffuse ([3], [12], [14], above discussion), we would like to argue that the functional dissociation in the amygdala could be based on the differential processing of elemental versus configural association. If this is true, then B may function as a primary amygdaloid processor for

Implications of the complexity hypothesis: remodelling associative fear conditioning

Based on investigations of the neural basis of fear conditioning in rodents, prevailing theories of amygdala refer either to the LA (e.g., Ref. [40]) or the entire BLA complex (e.g., Ref. [66]) as the principal site of convergence of neural pathways that carry information about CSs and USs. The above evidence and discussion imply, however, that this conception needs to be modified when discussing complex, configural CSs, such as an environmental context. In particular, it must be considered

Beyond S-R: an extended role of the amygdala

The amygdala integrates information from the external and internal milieu and has direct output connections to nuclei that control physiologic, autonomic and behavioural fear-induced responses. The evidence discussed thus far suggests that a consideration of the complexity dimension of motivational stimuli as well as that of the emotional responses may contribute to our understanding of the functional anatomy of the amygdala. What is clearly missing in the picture as presented, however, is how

Conclusion

The results reviewed here support the notion that functionally dissociable amygdala subsystems are involved in associative processes underlying aversive and possibly, appetitive emotional behavior. We suggest that in this dissociation, a complexity dimension may be an organizing factor both of input and output pathways of the amygdala. Yet, the potential variability of emotional responses to motivational stimuli of varying degrees of complexity assumes an important role for intra-amygdala

Acknowledgements

The authors thank Prof. Joseph LeDoux (NYU) for valuable comments.

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    1

    Present address: Center for Neurobiology and Behavior, Columbia University, New York, NY 10032, USA.

    2

    D.Y. and A.D. contributed equally to the work.

    3

    Present address: The Weizmann Institute of Science, Department of Neurobiology, Brain Research Building, Rehovot 76100, Israel.

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