Amygdalar roles during exposure to a live predator and to a predator-associated context

doi:10.1016/j.neuroscience.2010.10.033

Neuroscience

Volume 172, 13 January 2011, Pages 314-328

https://doi.org/10.1016/j.neuroscience.2010.10.033 Get rights and content

Abstract

The amygdala plays a critical role in determining the emotional significance of sensory stimuli and the production of fear-related responses. Large amygdalar lesions have been shown to practically abolish innate defensiveness to a predator; however, it is not clear how the different amygdalar systems participate in the defensive response to a live predator. Our first aim was to provide a comprehensive analysis of the amygdalar activation pattern during exposure to a live cat and to a predator-associated context. Accordingly, exposure to a live predator up-regulated Fos expression in the medial amygdalar nucleus (MEA) and in the lateral and posterior basomedial nuclei, the former responding to predator-related pheromonal information and the latter two nuclei likely to integrate a wider array of predatory sensory information, ranging from olfactory to non-olfactory ones, such as visual and auditory sensory inputs. Next, we tested how the amygdalar nuclei most responsive to predator exposure (i.e. the medial, posterior basomedial and lateral amygdalar nuclei) and the central amygdalar nucleus (CEA) influence both unconditioned and contextual conditioned anti-predatory defensive behavior. Medial amygdalar nucleus lesions practically abolished defensive responses during cat exposure, whereas lesions of the posterior basomedial or lateral amygdalar nuclei reduced freezing and increased risk assessment displays (i.e. crouch sniff and stretch postures), a pattern of responses compatible with decreased defensiveness to predator stimuli. Moreover, the present findings suggest a role for the posterior basomedial and lateral amygdalar nuclei in the conditioning responses to a predator-related context. We have further shown that the CEA does not seem to be involved in either unconditioned or contextual conditioned anti-predatory responses. Overall, the present results help to clarify the amygdalar systems involved in processing predator-related sensory stimuli and how they influence the expression of unconditioned and contextual conditioned anti-predatory responses.

Research Highlights

▶Predatory threat is processed by two parallel channels in the amygdala. ▶Lesions of the MEA practically abolish antipredatory-defense. ▶Lesions of the BMAp and LA reduce antipredatory-defense. ▶Both MEA and BMAp/LA pathways are involved in contextual conditioning. ▶Lesions of the CEA do not affect anti-predatory responses.

Section snippets

Animals and housing

Adult male Wistar rats (n=75), weighing about 250 g and obtained from the local breeding facilities, were used in the present study. The animals were kept under controlled temperature (23 °C) and illumination (12 h cycle) in the animal quarters, and had free access to water and standard laboratory diet.

Experiments were carried out in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals (NIH Publications No. 80-23, 1996). All experimental procedures

Experiment 1

The detailed behavioral analysis for this experimental group has been described elsewhere (Ribeiro-Barbosa et al., 2005, Cezario et al., 2008). In short, the three different phases of the experimental procedure provided, respectively, a low defensive baseline (Phase 1), where animals showed a great deal of nondefensive locomotion and other investigatory activities; a high level of freezing during cat exposure (Phase 2); and a high level of risk assessment (i.e. crouch-sniff and stretch

Discussion

In the present study, we made a systematic investigation to portray how the different amygdalar sites respond to a live predator or an environment previously associated with a predator, and tested how the amygdalar nuclei most responsive to predator exposure (i.e. the medial, posterior basomedial and lateral amygdalar nuclei) and the CEA influence both unconditioned and conditioned anti-predatory defensive behavior.

Cat exposure induced a significant increase in Fos levels in distinct amygdalar

Acknowledgments

This research was supported by grants from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, no. 05/59286-4) and Conselho Nacional de Desenvolvimento Científico e Tecnológico awarded to N.S.C. R.C.M., E.F.C.N. and E.R.R.B. were supported by FAPESP fellowships.

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Cognitive, Behavioral, and Systems NeuroscienceAmygdalar roles during exposure to a live predator and to a predator-associated context

Abstract

Research Highlights

Section snippets

Animals and housing

Experiment 1

Discussion

Acknowledgments

Neurosci Biobehav Rev

Pharmacol Biochem Behav

Neurobiol Learn Mem

Neuron

Neuroscience

Physiol Behav

Brain Res

Neuroscience

Neuron

Brain Res

Physiol Behav

Brain Res

Brain Res

Prog Neurobiol

Neuroscience

Behav Brain Res

Brain Res

Neurosci Biobehav Rev

Psychoneuroendocrinology

Neurosci Biobehav Rev

Neuroscience

Behav Brain Res

Brain Res

Innate and conditioned reactions to threat in rats with amygdaloid lesions

J Comp Physiol Psychol

Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex

Behav Neurosci

Perirhinal and postrhinal cortices of the rat: a review of the neuroanatomical literature and comparison with findings from the monkey brain

Hippocampus

Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat

J Comp Neurol

Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat

J Comp Neurol

Hypothalamic sites responding to predator threats—the role of the dorsal premammillary nucleus in unconditioned and conditioned antipredatory defensive behavior

Eur J Neurosci

The role of the amygdala in conditioned and unconditioned fear and anxiety

Cognitive, Behavioral, and Systems Neuroscience
Amygdalar roles during exposure to a live predator and to a predator-associated context