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Neural Regulation of the Stress Response: The Many Faces of Feedback
Open accessAbstract
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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“Dysfunctional GCC signaling is implicated in chronic pain disorders, such as fibromyalgia and neuropathic pain, where alterations in GCC expression or sensitivity may influence the body’s ability to control inflammation and modulate the nociceptive response [135].”
From The Role of Cortisol in Chronic Stress, Neurodegenerative Diseases, and Psychological Disorders (2023) · cites this paper as [135]
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“The GCC is essential for modulating the anti-inflammatory and immunosuppressive actions of cortisol [135].”
From The Role of Cortisol in Chronic Stress, Neurodegenerative Diseases, and Psychological Disorders (2023) · cites this paper as [135]
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Cited by
Sorted by citations
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Self-citationStress-induced sensitization: the hypothalamic–pituitary–adrenal axis and beyond
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“In contrast, the GR is only extensively occupied at high circulating glucocorticoid levels, and is the major mediator of negative feedback (Myers et al., 2012).”
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Schaeuble, D., & Myers, B. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.820398 · Cited by 50
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“In the mPFC, GR activation is involved with glucocorticoid negative feedback, but in the amygdala, it provides feedforward regulation of the HPA axis (Herman et al., 2016; Myers et al., 2012).”
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“Based on current evidence, the dlPFC—a key structure within the CEN—appears to be the best-supported target for addressing EF-related effects of stressors.”
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“GCs also elicit rapid nongenomic actions via activation of membrane receptors in the PVN (245,376).”
Nguyen, E. T., Streicher, J., Berman, S., Caldwell, J. L., Ghisays, V., Estrada, C. M., Wulsin, A. C., & Solomon, M. B. (2017) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.01.020 · Cited by 38
“responsiveness and restoration of homeostasis via the glucocorticoidmediated negative feedback [4].”
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Genetic Factors Mediate the Impact of Chronic Stress and Subsequent Response to Novel Acute Stress
Terenina, E. E., Cavigelli, S. A., Mormède, P., Zhao, W., Parks, C., Lu, L., Jones, B. C., & Mulligan, M. K. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00438 · Cited by 31
“Negative feedback regulation by glucocorticoids occurs both rapidly and over a longer time scale affected by previous stress experience (Myers et al., 2012).”
BackgroundMyers, B., McKlveen, J. M., Morano, R. L., Ulrich‐Lai, Y. M., Solomon, M. B., Wilson, S. P., & Herman, J. P. (2017) · Endocrinology · doi:10.1210/en.2017-00426 · Cited by 33
“neural, behavioral, and metabolic aspects of homeostasis (6).”
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“…is regulated via different pathways, including indirect projections from the amygdala to the hypothalamic paraventricular nucleus (Herman, et al., 2003; Myers, et al., 2012) and other alternative pathways that could differently impact the HPA axis reactivity in the absence of a functional amygdala.”
BackgroundThe stress of Arctic warming on polar bears
Boonstra, R., Bodner, K., Bosson, C. O., Delehanty, B., Richardson, E. S., Lunn, N. J., Derocher, A. E., & Molnár, P. K. (2020) · Global Change Biology · doi:10.1111/gcb.15142 · Cited by 32
Lifelong Aerobic Exercise Reduces the Stress Response in Rats
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“…in neural activation and/or mRNA expression of stress neuropeptides in limbic-forebrain regions that are involved in HPA regulation (Herman et al., 2005; Myers et al., 2012)—the medial prefrontal cortex (mPFC), amygdala, hippocampus and hypothalamus (Raineki et al., 2014; Lan et al., 2015).”
BackgroundGouveia, M. K., Miguel, T. T., Busnardo, C., Scopinho, A. A., Corrêa, F. M. D. A., Nunes‐de‐Souza, R. L., & Crestani, C. C. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.10.018 · Cited by 29
“…as a relay station between limbic processing of emotional information and elaboration of physiological and behavioral responses to stress (Adhikari, 2014; Choi et al., 2007; M AN US CR IP T AC CE PT ED ACCEPTED MANUSCRIPT 13 Crestani et al., 2013; Myers et al., 2012; Ulrich-Lai and Herman, 2009).”
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“, 2008), with GR being of particular importance in mediating glucocorticoid feedback inhibition of the HPA axis (Myers et al., 2012).”
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“, 2012 [77] for a review of feedback mechanisms).”
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“In both, CORT translocates to the nucleus coupled to a GR and inhibit the transcription of CRH and ACTH genes, decreasing the signal to continue the stress response.”
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“This response is regulated by negative and positive feedback mechanisms, where glucocorticoids (GCs) released from the adrenal gland can inhibit or stimulate (respectively) their own genomic and non-genomic actions by binding to glucocorticoid receptors (GRs) in the brain [7,8].”
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“These changes in glucocorticoid-metabolizing enzymes and receptor genes indicate an enhanced negative feedback regulation of the HPA axis to control and maintain glucocorticoid homeostasis (Myers et al., 2012).”
Subdiaphragmatic vagotomy enhances stress-induced epinephrine release in rats
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“For example, glucocorticoids have been found to exert a direct, inhibitory influence on the activity of the hypothalamic–pituitary–adrenal (HPA) axis at the level of the central nervous system (Myers et al., 2012; Tasker et al., 2011).”
BackgroundRaineki, C., Morgan, E., Ellis, L. A., & Weinberg, J. (2019) · Brain Research · doi:10.1016/j.brainres.2019.05.019 · Cited by 19
“Activation of GR in the amygdala, including the central nuclei, has been implicated in mediating the positive feedback loop that potentiates the activity of the HPA axis (Myers et al., 2012).”
BackgroundInfluentialSocial sleepers: The effects of social status on sleep in terrestrial mammals
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Anti-stress Properties of Atypical Antipsychotics
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“In this regard, glucocorticoids act as potent negative regulators of the HPA axis activity: by binding to their receptors in different structures, glucocorticoids extinguish the HPA axis response [39,41].”
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Nuclei-specific hypothalamus networks predict a dimensional marker of stress in humans
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“When these circuits trigger autonomic and endocrine stress responses, brainstem centres as well as the hypothalamic-pituitary-adrenal (HPA) are activated 8,9,13 .”
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Stress system and related biomarkers in Parkinson's disease
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Regulation of 11β-Hydroxysteroid Dehydrogenase Type 1 and 7α-Hydroxylase CYP7B1 during Social Stress
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“These structures express glucocorticoid receptors that contribute to feedback control of the HPA axis [6].”
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“This mechanism protects the body from the adverse effects of elevated cortisol, which are not limited to inflammation, muscle break - down, or immune suppression [45, 47].”
Metadata
- Authors
- Myers, B., McKlveen, J. M., & Herman, J. P.
- Affiliations
- University of Cincinnati (US)
- Corresponding author
- Myers, Brent
- Venue
- Cellular and Molecular Neurobiology
- Published
- 2012-02-01
- Volume
- 32
- Issue
- 5
- Pages
- 683-694
- ISSN
- 0272-4340 (ISSN-L)
- 1573-6830
- PMC
- PMC3956711
- OpenAlex
- W2004982081
- Semantic Scholar
- ab6597d145f936c7638a64a02075f0bd9d576ebc
- Cited by
- 175
- References
- 151
- Citations by year
- 2026: 5 · 2025: 13 · 2024: 8 · 2023: 10 · 2022: 23 · 2021: 10 · 2020: 13 · 2019: 11 · 2018: 16 · 2017: 11 · 2016: 14 · 2015: 15 · 2014: 12 · 2013: 11 · 2012: 3
- FWCI
- 5.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Cellular and Molecular Neurobiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH049698, R21MH090574, R01MH069860, R01MH069725)
- National Institute of Diabetes and Digestive and Kidney Diseases (T32DK059803)
- National Institute of Neurological Disorders and Stroke (T32NS007453)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Keywords
- stress response, glucocorticoids, hypothalamic-pituitary-adrenal axis, paraventricular nucleus, glucocorticoid receptor, cannabinoid signaling, mRNA degradation, neuropeptide signaling, homeostasis, brainstem
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