Cited by 105Stress Responses and CortisolNeuropeptides and Animal PhysiologyAdrenal Hormones and Disorders

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Sensitivity to glucocorticoid-mediated fast-feedback regulation of the hypothalamic–pituitary–adrenal axis is dependent upon stressor specific neurocircuitry

Thrivikraman, K.V, Nemeroff, Charles B, Plotsky, Paul M·2000·Brain Research

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Abstract

Unlabelled Fos-protein immunoreactivity (Fos-IR) was used to identify neurocircuits potentially participating in the regulation of hypothalamic-pituitary-adrenal (HPA) axis sensitivity to glucocorticoid-mediated fast-feedback in rats exposed to the physical stressor, hemorrhage, or the psychological stressor, airpuff startle. Marked regional brain differences in the Fos-IR expression were observed in response to these stressors. Specifically, after hemorrhage, nuclear Fos-IR increased in the nucleus of the solitary tract and other brainstem regions known to regulate hemodynamic processes including the supraoptic nucleus, and the magnocellular division of hypothalamic paraventricular nucleus (PVN). In contrast, after airpuff startle Fos-IR increased in the dorsomedial and lateral hypothalamus as well as in the lateral septum. Thus, activation of brainstem neurocircuits predominated after hemorrhage whereas activation of forebrain neurocircuits predominated after airpuff startle. In other regions, the magnitude of stressor-induced Fos-IR expression varied in a region-specific manner. When stressor exposure was preceded by administration of corticosterone to achieve levels within the physiological range after stressors, HPA axis responses were suppressed in response to the airpuff startle but not to either a small or moderate hemorrhage.In conclusion (1) fast-feedback mediated inhibition of HPA axis activity is critically dependent upon stressor modality; (2) this apparent selectivity is reflected by differences in the nature of the neurocircuitry mediating these stressors. It is suggested that determination of the central actions of glucocorticoids in mediating fast-feedback regulation of the HPA axis requires evaluation of the interactions between activated glucocorticoid receptors and intracellular signaling cascades evoked by convergent neuronal input.

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MethodSelf-citation
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Gonzales, M. M., Garrett, C. C., Chapman, C. D., & Dess, N. K. (2008) · Biological Psychology · doi:10.1016/j.biopsycho.2008.04.011 · Cited by 27
“Thus, CORT could play a role in stressinduced attenuation in LoS rats, possibly through fast-feedback downregulation of the HPA axis (Thrivikraman et al., 2000 ).”
Examining Stress Reactivity in Neonates: Relations Between Cortisol and Behavior
Keenan, K. E., Grace, D., & Gunthorpe, D. (2003) · Child Development · doi:10.1046/j.1467-8624.2003.00647.x · Cited by 27
Role of catecholaminergic inputs to the medial prefrontal cortex in local and subcortical expression of Fos after psychological stress
Spencer, S. J., & Day, T. A. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20242 · Cited by 27
“This procedure has been shown previously to induce behavioral responses (Duncan et al., 1996), neuronal activation (Thrivikraman et al., 2000; Spencer et al., 2004), and elevations in plasma pituitary-adrenal hormones (Thrivikraman et al., 2000) typical of those seen with other psychological…”
BackgroundMethodInfluential
Magnocellular vasopressin and the mechanism of “Glucocorticoid escape”
Antoni, F. A. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00422 · Cited by 26
“Subsequently, these workers showed that HPA activation by airpuff startle, a psychological stressor, was sensitive to inhibition by corticosterone whereas that caused by small or moderate hemorrhage was not (41).”
Background
Activation of 5-HT 1A receptors in the rat dorsomedial hypothalamus inhibits stress-induced activation of the hypothalamic–pituitary–adrenal axis
Stamper, C. E., Hassell, J. E., Kapitz, A. J., Renner, K. J., Orchinik, M., & Lowry, C. A. (2017) · Stress · doi:10.1080/10253890.2017.1301426 · Cited by 26
“The DMH may preferentially process information relevant to exteroceptive or “emotional” rather than interoceptive or “physical” stressors, and plays an important role in the control of stress-induced HPA axis activity (DiMicco et al., 2002; Ebner et al., 2013; Thrivikraman et al., 2000).”
Background
Stress-induced glucocorticoid desensitizes adrenoreceptors to gate the neuroendocrine response to somatic stress in male mice
Jiang, Z., Chen, C., Weiss, G. L., Fu, X., Stelly, C. E., Sweeten, B. L. W., Tirrell, P. S., Pursell, I. A., Stevens, C. R., Fisher, M. O., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111509 · Cited by 26
“Note that systemic corticosterone injection failed to suppress the HPA response to the somatic stress induced by a salt load (Thrivikraman et al., 2000).”
Rapid alteration of stress-induced hypothalamic–pituitary–adrenal hormone secretion in the rat: A comparison of glucocorticoids and cannabinoids
Ginsberg, A. B., Pecoraro, N. C., Warne, J. P., Horneman, H. F., & Dallman, M. F. (2010) · Stress · doi:10.3109/10253890903336839 · Cited by 24
“The faster inhibition (seconds or minutes, up to 1 h) has been demonstrated convincingly by a number of researchers (Keller-Wood and Dallman 1984; Liberzon et al. 1997; Thrivikraman et al. 2000), but the underlying mechanism and dynamics have not been definitively characterized in vivo.”
Background
Differential gene expression in WKY and SHR brain following acute and chronic air-puff stress
McDougall, S. J., Widdop, R. E., & Lawrence, A. J. (2004) · Molecular Brain Research · doi:10.1016/j.molbrainres.2004.10.010 · Cited by 23
Role of the dorsomedial hypothalamus in glucocorticoid-mediated feedback inhibition of the hypothalamic–pituitary–adrenal axis
Stamper, C. E., Hennessey, P. A., Hale, M. W., Lukkes, J. L., Donner, N. C., Lowe, K. R., Paul, E. D., Spencer, R. L., Renner, K. J., Orchinik, M., et al. (2015) · Stress · doi:10.3109/10253890.2015.1004537 · Cited by 19
“The dorsomedial hypothalamus (DMH) is a target for the rapid actions of corticosteroids (Feng et al., 2009; Gasser et al., 2006; Lowry et al., 2001; Thrivikraman et al., 2000) and appears to be involved in integrating stress-related signals with neuroendocrine, autonomic and behavioral output (Bernardis & Bellinger, 1…”
BackgroundInfluential
Functional plasticity of cyclic AMP hydrolysis in rat adenohypophysial corticotroph cells
Ang, K.-L., & Antoni, F. A. (2002) · Cellular Signalling · doi:10.1016/s0898-6568(01)00267-4 · Cited by 20
Inhibitory Function of the Dorsomedial Hypothalamic Nucleus on the Hypothalamic–Pituitary–Adrenal Axis Response to an Emotional Stressor but not Immune Challenge
Ebner, K., Muigg, P., & Singewald, N. (2013) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02369.x · Cited by 18
Single-unit activity of paraventricular nucleus neurons in response to intero- and exteroceptive stressors in conscious, freely moving rats
Watanabe, S., Kunitake, T., Kato, K., Chu, C., Nakao, H., Qiu, D., & Kannan, H. (2003) · Brain Research · doi:10.1016/j.brainres.2003.09.058 · Cited by 13
“Thus, water deprivation can be considered a prototypical systemic, interoceptive stressor [42,52].”
Influential
Clozapine prevented social interaction deficits and reduced c-Fos immunoreactivity expression in several brain areas of rats exposed to acute restraint stress
de Oliveira, R. P., de Andrade, J. S., Spina, M., Chamon, J. V., Silva, P. H. D., Werder, A. K., Ortolani, D., Thomaz, L. D. S. C., Romariz, S. A. A., Ribeiro, D. A., et al. (2022) · PLoS ONE · doi:10.1371/journal.pone.0262728 · Cited by 13
“In addition, 10 min of immobilization in rats elevated extracellular levels of 5-hydroxyindoleacetic acid (5-HIAA) a 5-HT metabolite in the PFC, CA3 and MnR [59]; (iii) LS receives pronounced projections from the MnR [60], and innervates the peri-PVN region [61] participating in the regulation of the HPA axis activity…”
Background
Ingestion of non-caloric liquid diet is sufficient to restore plasma corticosterone level, but not to induce the hypothalamic c-Fos expression in food-deprived rats
Yoo, S. B., Lee, J.-H., Ryu, V., & Jahng, J. W. (2007) · Nutritional Neuroscience · doi:10.1080/10284150701723859 · Cited by 9
“Plasma level of glucocorticoids is elevated as a consequence of the HPA axis activation responding to stress, and various stressors induce c-Fos expression in the PVN neurons (Emmert and Herman 1999; Thrivikraman et al. 2000; Figueiredo et al. 2003; Crane et al. 2005; Yanagita et al. 2007).”
Background
Stress and Reproduction in Mammals
Uphouse, L. L. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-374928-4.10007-0 · Cited by 9
Exposure to mild stress and brain derived neurotrophin factor (BDNF) immunoreactivity in the hypothalamic paraventricular (PVN) and supraoptic (SON) nuclei: Comparison between aged and adult rats
Badowska‐Szalewska, E., Ludkiewicz, B., Krawczyk, R., & Moryś, J. (2016) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2016.08.007 · Cited by 9
Comparison of the influence of two models of mild stress on hippocampal brain‑derived neurotrophin factor (BDNF) immunoreactivity in old age rats
Badowska‐Szalewska, E., Ludkiewicz, B., Krawczyk, R., Melka, N., & Moryś, J. (2017) · Acta Neurobiologiae Experimentalis · doi:10.21307/ane-2017-037 · Cited by 9
“OF in PVN; c‑Fos is a marker of neuronal/trans‑synaptic activations – Kovács 1998, Thrivikraman et al. 2000) (see Badowska‑Szalewska et al. 2016b, supplementary data).”
Background
The immunoreactivity of c-Fos, NGF and its receptor TrkA after open-field exposure in the central and medial nuclei of the rat amygdala.
Badowska‐Szalewska, E., Ludkiewicz, B., Domaradzka-Pytel, B., Dziewíatkowski, J., Spodnik, J. H., & Moryś, J. (2006) · PubMed · Cited by 9
Stress-induced changes of interleukin-1beta within the limbic system in the rat.
Badowska‐Szalewska, E., Klejbor, I., Sidor-Kaczmarek, J., Cecot, T., Lietzau, G., Spodnik, J. H., & Moryś, J. (2009) · PubMed · Cited by 8
The impact of two mild stressors on the nerve growth factor (NGF) immunoreactivity in the amygdala in aged rats compared to adult ones
Badowska‐Szalewska, E., Ludkiewicz, B., Krawczyk, R., & Moryś, J. (2015) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2015.12.005 · Cited by 7
“On the other hand, the level of HPA activation can be evaluated on the basis of c-Fos-ir neuron density (c-Fos-ir can be used as an index of neuronal/trans-synaptic activations in the stress-related circuitry – Kovács, 1998; Thrivikraman et al., 2000) in PVN.”
Background
Hypothalamic-Pituitary-Adrenal Axis
Gabry, K. E., Gold, P. W., & Chrousos, G. P. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50083-4 · Cited by 7
Estrogen receptors ERα and ERβ participation in hypothalamus–pituitary–adrenal axis activation by hemorrhagic stress
Alves, L. M. S., Filho, P. C. G. D. B., & Franci, C. R. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.03.001 · Cited by 5
Hypothalamic–Pituitary–Adrenal Cortical Axis
Rhodes, M. E., McKlveen, J. M., Ripepi, D. R., & Gentile, N. E. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00073-5 · Cited by 5
Rapid Corticosteroid Actions on Behavior: Mechanisms and Implications
Gasser, P. J., Lowry, C. A., & Orchinik, M. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00041-3 · Cited by 5
Locus Coeruleus Noradrenergic Modulation of Diurnal Corticosterone, Stress Reactivity, and Cardiovascular Homeostasis in Male Rats
Thrivikraman, K. V., Kinkead, B. L., Owens, M. J., Rapaport, M. H., & Plotsky, P. M. (2021) · Neuroendocrinology · doi:10.1159/000520192 · Cited by 4
Self-citation
Immunoreactivity of c-Fos, NGF and its receptor TrkA in the periventricular zone of the rat hypothalamus after open field exposure.
Badowska‐Szalewska, E., Klejbor, I., Ludkiewicz, B., Domaradzka-Pytel, B., Dziewíatkowski, J., Spodnik, J. H., & Moryś, J. (2006) · PubMed · Cited by 4
Embedded Synaptic Feedback in the Neuroendocrine Stress Axis
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Stress and Spatial Maze Performance in the Rat
Taylor, S. B., Conrad, C. D., & Olive, M. F. (2014) · Neuromethods · doi:10.1007/978-1-4939-2159-1_8 · Cited by 2
Stress and Reproduction in Mammals
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The utilization of the climatic chamber to evaluate the influence of ambient conditions on endocrine, nervous and immune systems of rats.
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New Vistas of Old Terrains: Magnocellular Vasopressin and the Neuroendocrine Response to Stress
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Brain changes underlying the long-term effects of a single previous exposure to emotional or systemic stressors in rats a view from the hypothalamic-pituitary-adrenal axis
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Variations in adrenal hormones in law enforcement servicemen during a mission to local armed conflict
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Participação de receptores ER e ER na ativação do eixo hipotálamo-hipófise-adrenal por estresse hemorrágico
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Central Mechanisms Regulating Pituitary-Adrenal Activity in Infant Guinea Pigs (Cavia porcellus) during Exposure to Psychological Stressors: Independent and Combined Effects of Maternal Separation and Novelty
Maken, D. S. (2009) · OhioLink ETD Center (Ohio Library and Information Network)
Age-Related (Aged vs. Adult) Comparison of the Effect of Two Mild Stressors on the Nerve Growth Factor (NGF) in the Rat Hypothalamic Supraoptic Nucleus (SON) – Immunohistochemical Study
Badowska‐Szalewska, E., Ludkiewicz, B., Krawczyk, R., & Moryś, J. (2016) · Folia Biologica · doi:10.14712/fb2016062050212
“Indirectly, it is supported by the fact that the density of the c-Fos-ir cells (c-Fos expression can be taken as an index of neuronal/trans-synaptic activations in the stress-related circuitry – Kovács, 1998; Thrivikraman et al., 2000) in PVN, which is the site where HPA axis activation is initiated, was higher in the…”
Background
Neural circuitry involved in physiological responses following acute and repeated psychological stress: role of the anterior posterior hypothalamus
Nyhuis, T. J. (2013) · CU Scholar (University of Colorado Boulder)
Consequences of maternal abuse on HPA axis function, growth, and social and stress-induced behavior in juvenile rhesus macaques
Grand, A. P. (2008)

Authors: Thrivikraman, K. V., Nemeroff, C. B., & Plotsky, P. M.
Affiliations: Emory University (US)
Corresponding author: Thrivikraman, K.V
ORCID: Nemeroff, Charles B
Venue: Brain Research
Publisher: Elsevier BV
Published: 2000-07
Volume: 870
Issue: 1-2
Pages: 87-101
ISSN: 0006-8993 (ISSN-L)
DOI: 10.1016/s0006-8993(00)02405-7
OpenAlex: W2033574728
Cited by: 105
References: 135
Citations by year: 2022: 3 · 2021: 3 · 2020: 1 · 2019: 4 · 2017: 3 · 2016: 6 · 2015: 6 · 2014: 4 · 2013: 1 · 2012: 2
FWCI: 3.47
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Brain Research (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Mental Health (R01MH042088, MH42088, MH-OD51745)
National Institute of Diabetes and Digestive and Kidney Diseases (DK-33093)
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: hypothalamic-pituitary-adrenal axis, glucocorticoid negative feedback, Fos expression, stressor specificity, nucleus tractus solitarius, hypothalamus, lateral septum, corticosterone, glucocorticoid receptor, stress response
MeSH terms: Air Movements, Animals, Consciousness, Feedback, Glucocorticoids, Hemorrhage, Hypothalamo-Hypophyseal System, Male, Neural Pathways, Paraventricular Hypothalamic Nucleus, Pituitary-Adrenal System, Receptors, Glucocorticoid, Reflex, Startle, Stress, Psychological, Proto-Oncogene Proteins c-fos, Rats, Sprague-Dawley, Hypovolemia, Rats

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Sensitivity to glucocorticoid-mediated fast-feedback regulation of the hypothalamic–pituitary–adrenal axis is dependent upon stressor specific neurocircuitry

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