Habituation to repeated restraint stress is associated with lack of stress-induced c-fos expression in primary sensory processing areas of the rat brain

M. Girotti, Thaddeus Wesley Warren Pace, R. I. Gaylord, B. A. Rubin, J. P. Herman, R. L. Spencer

Research output: Contribution to journalArticle

165 Citations (Scopus)

Abstract

Rats repeatedly exposed to restraint show a reduced hypothalamic-pituitary- adrenal axis response upon restraint re-exposure. This hypothalamic-pituitary- adrenal axis response habituation to restraint does not generalize to other novel stressors and is associated with a decrease in stress-induced c-fos expression in a number of stress-reactive brain regions. We examined whether habituation to repeated restraint is also associated with adaptation of immediate early gene expression in brain regions that process and relay primary sensory information. These brain regions may not be expected to show gene expression adaptation to repeated restraint because of their necessary role in experience discrimination. Rats were divided into a repeated restraint group (five 1-hour daily restraint sessions) and an unstressed group (restraint naïve). On the sixth day rats from each group were either killed with no additional stress experience or at 15, 30 or 60 min during restraint. Immediate early gene expression (corticotrophin-releasing hormone heteronuclear RNA, c-fos mRNA, zif268 mRNA) was determined by in situ hybridization. A reduction in stress-induced hypothalamic-pituitary-adrenal axis hormone secretion (plasma corticosterone and adrenocorticotropic hormone) and immediate early gene expression levels in the paraventricular nucleus of the hypothalamus, the lateral septum and the orbital cortex was observed in repeated restraint as compared with restraint naïve animals. This reduction was already evident at 15 min of restraint. Unexpectedly, we also found in repeated restraint rats a reduction in restraint-induced c-fos expression in primary sensory-processing brain areas (primary somatosensory cortex, and ventroposteriomedial and dorsolateral geniculate nuclei of thalamus). The overall levels of hippocampal mineralocorticoid receptor heteronuclear RNA or glucocorticoid receptor mRNA were not decreased by repeated restraint, as may occur in response to severe chronic stress. We propose that repeated restraint leads to a systems-level adaptation whereby re-exposure to restraint elicits a rapid inhibitory modulation of primary sensory processing (i.e. sensory gating), thereby producing a widespread attenuation of the neural response to restraint.

Original languageEnglish (US)
Pages (from-to)1067-1081
Number of pages15
JournalNeuroscience
Volume138
Issue number4
DOIs
StatePublished - 2006
Externally publishedYes

Fingerprint

Immediate-Early Genes
Gene Expression
Brain
Messenger RNA
RNA
Sensory Gating
Lateral Hypothalamic Area
Geniculate Bodies
Mineralocorticoid Receptors
Somatosensory Cortex
Paraventricular Hypothalamic Nucleus
Corticotropin-Releasing Hormone
Glucocorticoid Receptors
Corticosterone
Prefrontal Cortex
Thalamus
Adrenocorticotropic Hormone
In Situ Hybridization
Hormones

Keywords

  • HPA axis
  • Immediate early genes
  • In situ hybridization

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Habituation to repeated restraint stress is associated with lack of stress-induced c-fos expression in primary sensory processing areas of the rat brain. / Girotti, M.; Pace, Thaddeus Wesley Warren; Gaylord, R. I.; Rubin, B. A.; Herman, J. P.; Spencer, R. L.

In: Neuroscience, Vol. 138, No. 4, 2006, p. 1067-1081.

Research output: Contribution to journalArticle

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abstract = "Rats repeatedly exposed to restraint show a reduced hypothalamic-pituitary- adrenal axis response upon restraint re-exposure. This hypothalamic-pituitary- adrenal axis response habituation to restraint does not generalize to other novel stressors and is associated with a decrease in stress-induced c-fos expression in a number of stress-reactive brain regions. We examined whether habituation to repeated restraint is also associated with adaptation of immediate early gene expression in brain regions that process and relay primary sensory information. These brain regions may not be expected to show gene expression adaptation to repeated restraint because of their necessary role in experience discrimination. Rats were divided into a repeated restraint group (five 1-hour daily restraint sessions) and an unstressed group (restraint na{\"i}ve). On the sixth day rats from each group were either killed with no additional stress experience or at 15, 30 or 60 min during restraint. Immediate early gene expression (corticotrophin-releasing hormone heteronuclear RNA, c-fos mRNA, zif268 mRNA) was determined by in situ hybridization. A reduction in stress-induced hypothalamic-pituitary-adrenal axis hormone secretion (plasma corticosterone and adrenocorticotropic hormone) and immediate early gene expression levels in the paraventricular nucleus of the hypothalamus, the lateral septum and the orbital cortex was observed in repeated restraint as compared with restraint na{\"i}ve animals. This reduction was already evident at 15 min of restraint. Unexpectedly, we also found in repeated restraint rats a reduction in restraint-induced c-fos expression in primary sensory-processing brain areas (primary somatosensory cortex, and ventroposteriomedial and dorsolateral geniculate nuclei of thalamus). The overall levels of hippocampal mineralocorticoid receptor heteronuclear RNA or glucocorticoid receptor mRNA were not decreased by repeated restraint, as may occur in response to severe chronic stress. We propose that repeated restraint leads to a systems-level adaptation whereby re-exposure to restraint elicits a rapid inhibitory modulation of primary sensory processing (i.e. sensory gating), thereby producing a widespread attenuation of the neural response to restraint.",
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