Does the amygdala modulate adaptation to repeated stress?

doi:10.1016/j.neuroscience.2004.01.018

Neuroscience

Volume 126, Issue 1, 2004, Pages 9-19

https://doi.org/10.1016/j.neuroscience.2004.01.018 Get rights and content

Abstract

Exposure of the rat to restraint results in activation of the hypothalamic–pituitary–adrenal (HPA) axis, a characteristic pattern of c-fos expression in the brain and increased cardiovascular function. These responses adapt with repeated exposure of an individual to the same stress. Corticosterone secretion habituates, and c-fos mRNA expression in the paraventricular nucleus of the hypothalamus (PVN) decreases. The increased expression of corticotropin releasing hormone mRNA in the PVN also becomes less prominent, whereas vasopressin mRNA progressively increases. The neural mechanisms responsible for this adaptation remain obscure. Because of its role in conditioned learning, we have hypothesised that the amygdala might be involved in this adaptive process. Here we show that large neurotoxic lesions of the amygdala in male rats do not prevent acute stress activation of the HPA axis following 30 min restraint, whilst more discrete lesions of the central nucleus actually exacerbate the acute response. Rats with large amygdala lesions demonstrate delayed habituation of corticosterone and c-fos to repeated restraint, an affect not apparent with central nucleus lesions. Furthermore we show that neither type of lesion significantly reduced tachycardiac responses to single or repeated restraint as measured by telemetry. We conclude that the amygdala and the central nucleus are not necessary for HPA and cardiovascular activation in response to stress (though the central nucleus may modulate it), and that adaptation to repeated stress is only modestly dependent upon the amygdala.

Section snippets

Animals

All procedures were carried out under Home Office (UK) licence; both numbers of animals and post-operative discomfort were minimized according to the conditions of the licence. Male Lister Hooded rats (Harlan, Bicester, UK) weighing between 200 and 250 g at the start of the experiment were used. They were housed in groups of five to six per cage, with ad libitum access to food and water, and were kept on a 12-h light/dark cycle with lights off at 10.00 a.m. Animals were handled daily for at

Results

The results from experiments 1A–2A are represented in Table 1. Data represented by figures are indicated.

Discussion

The proposition that adaptation to repeated stress is dependent on the amygdala has never been adequately tested previously. These experiments measured a range of responses to restraint stress, across neural, endocrine and autonomic dimensions. We used different neurotoxins to make larger, near ‘total’ amygdaloid lesions, or smaller, more localised central nucleus ones since, in our hands, each gave an appropriate level of control of lesion size. Though there are a priori reasons to suggest

Conclusions

The results presented here strongly suggest that the amygdala plays a minor role in the generation of physiological stress responses across a range of measures in the face of an unconditioned, largely psychological, threat. This implies that other pathways are used by the brain to generate stress in these contexts. Furthermore the data suggest that the process of adaptation to stress need not depend entirely upon the amygdala. Nonetheless there is evidence that the amygdala modulates the stress

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¹: Present address: Endocrinology Unit, Molecular Medicine Centre, Western General Hospital, Edinburgh EH4 2XU, UK.

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Does the amygdala modulate adaptation to repeated stress?

Abstract

Section snippets

Animals

Results

Discussion

Conclusions

Behav Brain Res

Prog Brain Res

Behav Brain Res

Neuroscience

Brain Res

Biol Psychiatry

Brain Res

Neurobiol Learn Mem

Physiol Behav

Behav Neural Biol

J Psychosom Res

Metabolism

Pharmacol Biochem Behav

Neuroscience

Control of ACTH secretion by the central nucleus of the amygdalaImplication of the serotoninergic system and its relevance to the glucocorticoid delayed negative feedback mechanism

Neuroendocrinology

Participation of the central amygdaloid nucleus in the response of adrenocorticotropin secretion to immobilization stressOpposing roles of the noradrenergic and dopaminergic systems

Neuroendocrinology

The role of stress and the hypothalamic-pituitary-adrenal axis in the pathogenesis of the metabolic syndromeNeuro-endocrine and target tissue-related causes

Int J Obes Relat Metab Disord

Stressor categorizationAcute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups

Eur J Neurosci

Neuroendocrine responses to an emotional stressorEvidence for involvement of the medial but not the central amygdala

Eur J Neurosci

Opposing roles for medial and central amygdala in the initiation of noradrenergic cell responses to a psychological stressor

Eur J Neurosci

Amygdalectomy inhibits adrenocortical responses to somatosensory and olfactory stimulation

Neuroendocrinology

Role of amygdala norepinephrine in mediating stress hormone regulation of memory storage

Acta Pharmacol Sin

Influence of amygdala lesions on cardiovascular responses to alerting stimuli, on behaviour and on blood pressure development in spontaneously hypertensive rats

Acta Physiol Scand