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Neural Regulation of the Stress Response: The Many Faces of Feedback

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Abstract

The mammalian stress response is an integrated physiological and psychological reaction to real or perceived adversity. Glucocorticoids (GCs) are an important component of this response, acting to redistribute energy resources to both optimize survival in the face of challenge and restore homeostasis after the immediate threat has subsided. Release of GCs is mediated by the hypothalamo–pituitary–adrenocortical (HPA) axis, driven by a neural signal originating in the paraventricular nucleus (PVN). Stress levels of GCs bind to glucocorticoid receptors (GRs) in multiple body compartments, including brain, and consequently have wide-reaching actions. For this reason, GCs serve a vital function in feedback inhibition of their own secretion. Fast, non-genomic feedback inhibition of the HPA axis is mediated at least in part by GC signaling in the PVN, acting by a cannabinoid-dependent mechanism to rapidly reduce both neural activity and GC release. Delayed feedback termination of the HPA axis response is mediated by forebrain GRs, presumably by genomic mechanisms. GCs also act in the brainstem to attenuate neuropeptidergic excitatory input to the PVN via acceleration of mRNA degradation, providing a mechanism to attenuate future responses to stressors. Thus, rather than having a single defined feedback switch, GCs work through multiple neurocircuits and signaling mechanisms to coordinate HPA axis activity to suit the overall needs of multiple body systems.

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Abbreviations

ACTH:

Adrenocorticotropin

BLA:

Basolateral amygdala

BST:

Bed nucleus of the stria terminalis

CB1:

Type 1 cannabinoid receptor

CeA:

Central nucleus of the amygdala

CRH:

Corticotropin-releasing hormone

DMH:

Dorsomedial hypothalamus

eCB:

Endocannabinoid

GC:

Glucocorticoid

GLP-1:

Glucagon-like peptide-1

GR:

Glucocorticoid receptor

GSE:

Glucocorticoid-induced suppression of excitation

HPA:

Hypothalamo–pituitary–adrenocortical

ilPFC:

Infralimbic prefrontal cortex

MDD:

Major depressive disorder

mGR:

Membrane-associated GR

mPFC:

Medial prefrontal cortex

MR:

Mineralocorticoid receptor

NTS:

Nucleus of the solitary tract

plPFC:

Prelimbic prefrontal cortex

POA:

Preoptic area

PPG:

Preproglucagon

PTSD:

Post-traumatic stress disorder

PVN:

Paraventricular nucleus

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Acknowledgments

The authors would like to acknowledge support from NIH grants DK059803 (BM), NS007453 (JMM), MH049698, MH069725, MH069860, and MH090574 (JPH). We are also grateful for the artistic contributions of Anne Christiansen and Nathan Evanson.

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  1. Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Metabolic Diseases Institute, 2170 E. Galbraith Rd, Cincinnati, OH, 45237-0506, USA

    Brent Myers, Jessica M. McKlveen & James P. Herman

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  1. Brent Myers
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  2. Jessica M. McKlveen
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  3. James P. Herman
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Correspondence to Brent Myers.

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Special Issue on Stress (Kvetnansky and Saavedra, Editors).

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Myers, B., McKlveen, J.M. & Herman, J.P. Neural Regulation of the Stress Response: The Many Faces of Feedback. Cell Mol Neurobiol 32, 683–694 (2012). https://doi.org/10.1007/s10571-012-9801-y

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