Limbic Regulation of Hypothalamo‐Pituitary‐Adrenocortical Function during Acute and Chronic Stress

Jankord, Ryan; Herman, James P.

doi:10.1196/annals.1410.012

Cited by 578Stress Responses and CortisolMemory and Neural MechanismsNeuropeptides and Animal Physiology

Limbic Regulation of Hypothalamo‐Pituitary‐Adrenocortical Function during Acute and Chronic Stress

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Jankord, Ryan, Herman, James P.·2008·Annals of the New York Academy of Sciences

DOI 10.1196/annals.1410.012PMC PMC2637449

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Abstract

The hypothalamo‐pituitary‐adrenocortical (HPA) axis is responsible for initiation of glucocorticoid stress responses in all vertebrate animals. Activation of the axis is regulated by diverse afferent input to the hypothalamic paraventricular nucleus (PVN). This review discusses brain mechanisms subserving generation and inhibition of stress responses focusing on the contribution of the limbic system and highlighting recent conceptual advances regarding organization of stress response pathways in the brain. First, control of HPA axis responses to psychogenic stimuli is exerted by a complex neurocircuitry that involves oligosynaptic networks between limbic forebrain structures and the PVN. Second, individual stress‐modulatory structures can have a heterogeneous impact on HPA axis responses, based on anatomical micro‐organization and/or stimulus properties. Finally, HPA axis hyperactivity pursuant to chronic stress involves a substantial functional and perhaps anatomical reorganization of central stress‐integrative circuits. Overall, the data suggest that individual brain regions do not merely function as monolithic activators or inhibitors of the HPA axis and that network approaches need be taken to fully understand the nature of the neuroendocrine stress response.

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Music listening prior to the experience of stress may add to, facilitate, or increase subsequent HPA axis activation by a staggered activation of a partly shared neuronal network.
“It appears that music listening prior to the experience of stress may add to, facilitate, or increase subsequent HPA axis activation by a staggered activation of a partly shared neuronal network.”
From The Effect of Music on the Human Stress Response (2013) · cites this paper as [78]
The paper’s Abstract reports that chronic stress can facilitate HPA-related responses to novel stressors and links stress responses to limbic pathways. It does not address music listening before stress or establish staggered activation of a partly shared neuronal network as the mechanism for an increased response. (LLM, conf=0.82)
Experimental — accuracy not yet measured
The hypothalamus coordinates stress responses partly by regulating peripheral glucocorticoid secretion.
“The hypothalamus coordinates stress responses, in part through the regulation of peripheral glucocorticoid secretion (95).”
From Neural mechanisms of ageing and cognitive decline (2010) · cites this paper as [95]
GCs are the principal end-products of the HPA axis, which help to maintain homeostatic balance in the organism.
“GCs are “the principal end-products of the HPA axis”, which help to maintain homeostatic balance in the organism (Jankord and Herman, 2008).”
From Glutamate receptors in domestication and modern human evolution (2020) · cites this paper as Jankord and Herman, 2008
GCs promote glutamate release in feedback regions, and the different affinities of mineralocorticoid receptors and glucocorticoid receptors enable the modulation of stress feedback signaling from basal or moderate to acute levels.
“GCs promote glutamate release in these feedback regions, and the different affinities of mineralocorticoid receptors (MRs; bound by GCs at low concentrations) and glucocorticoid receptors (GRs; bound at higher concentrations) enable the modulation of stress feedback signaling from basal or moderate to acute levels (Jankord and Herman, 2008;Herman et al., 2012).”
From Glutamate receptors in domestication and modern human evolution (2020) · cites this paper as Jankord and Herman, 2008

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Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation
REUL, J. M. H. M., & KLOET, E. R. D. (1985) · Endocrinology · doi:10.1210/endo-117-6-2505 · Cited by 2,580 · see citing works
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Sesack, S. R., Deutch, A. Y., Roth, R. H., & Bunney, B. S. (1989) · Journal of Comparative Neurology · doi:10.1002/cne.902900205 · Cited by 1,568 · see citing works
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Vertes, R. P. (2004) · Synapse · doi:10.1002/syn.10279 · Cited by 1,550 · see citing works
What is the amygdala?
Swanson, L. W., & Petrovich, G. D. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01265-x · Cited by 1,351 · see citing works
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Diorio, D., Viau, V, & Meaney, M. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03839.1993 · Cited by 1,151 · see citing works
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Cullinan, W. E., Herman, J. P., Battaglia, D. F., Akil, H., & Watson, S. J. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00355-9 · Cited by 1,056 · see citing works
Self-citation
Efferent projections of the infralimbic cortex of the rat
Hurley, K. M., Herbert, H., Moga, M. M., & Saper, C. B. (1991) · Journal of Comparative Neurology · doi:10.1002/cne.903080210 · Cited by 777 · see citing works
Topography of projections from amygdala to bed nuclei of the stria terminalis
Dong, H.-W., Petrovich, G. D., & Swanson, L. W. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00079-0 · Cited by 714 · see citing works
Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration
Wellman, C. L. (2001) · Journal of Neurobiology · doi:10.1002/neu.1079 · Cited by 594 · see citing works
Ventral subicular interaction with the hypothalamic paraventricular nucleus: Evidence for a relay in the bed nucleus of the stria terminalis
Cullinan, W. E., Herman, J. P., & Watson, S. J. (1993) · Journal of Comparative Neurology · doi:10.1002/cne.903320102 · Cited by 541 · see citing works
Self-citation
Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups
Dayas, C. V., Buller, K. M., Crane, J. W., Xu, Y., & Day, T. A. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01733.x · Cited by 514 · see citing works
Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress
Bhatnagar, S., & Dallman, M. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00577-0 · Cited by 511 · see citing works
Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner
Ulrich‐Lai, Y. M., Figueiredo, H. F., Ostrander, M. M., Choi, D. C., Engeland, W. C., & Herman, J. P. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00070.2006 · Cited by 497 · see citing works
Self-citation
Alterations in corticotropin-releasing factor-like immunoreactivity in discrete rat brain regions after acute and chronic stress
Chappell, P., Smith, M., Kilts, C., Bissette, G., Ritchie, J., Anderson, C., & Nemeroff, C. (1986) · The Journal of Neuroscience · doi:10.1523/jneurosci.06-10-02908.1986 · Cited by 464 · see citing works
Regulatory Changes in Neuroendocrine Stress-Integrative Circuitry Produced by a Variable Stress Paradigm
Herman, J. P., Adams, D. J., & Prewitt, C. M. (2008) · Neuroendocrinology · doi:10.1159/000126839 · Cited by 458 · see citing works
Self-citation
Regional Differentiation of the Medial Prefrontal Cortex in Regulating Adaptive Responses to Acute Emotional Stress
Radley, J. J., Arias, C. M., & Sawchenko, P. E. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4297-06.2006 · Cited by 456 · see citing works
Corticosterone effects on corticotropin-releasing hormone mRNA in the central nucleus of the amygdala and the parvocellular region of the paraventricular nucleus of the hypothalamus
Makino, S., Gold, P. W., & Schulkin, J. (1994) · Brain Research · doi:10.1016/0006-8993(94)91862-7 · Cited by 400 · see citing works
Bed Nucleus of the Stria Terminalis Subregions Differentially Regulate Hypothalamic–Pituitary–Adrenal Axis Activity: Implications for the Integration of Limbic Inputs
Choi, D. C., Furay, A. R., Evanson, N. K., Ostrander, M. M., Ulrich-Lai, Y. M., & Herman, J. P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4301-06.2007 · Cited by 392 · see citing works
Self-citation
Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior
Boyle, M. P., Brewer, J. A., Funatsu, M., Wozniak, D. F., Tsien, J. Z., Izumi, Y., & Muglia, L. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406458102 · Cited by 378 · see citing works
Lateralized Effects of Medial Prefrontal Cortex Lesions on Neuroendocrine and Autonomic Stress Responses in Rats
Sullivan, R. M., & Gratton, A. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-07-02834.1999 · Cited by 377 · see citing works
Chronic stress attenuates glucocorticoid negative feedback: involvement of the prefrontal cortex and hippocampus
Mizoguchi, K., Ishige, A., Aburada, M., & Tabira, T. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00105-2 · Cited by 369 · see citing works
Circuits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms
Sawchenko, P. E., Li, H.-Y., & Ericsson, A. B. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62131-7 · Cited by 353 · see citing works
Direct Projections from the Central Amygdaloid Nucleus to the Hypothalamic Paraventricular Nucleus: Possible Role in Stress-Induced Adrenocorticotropin Release
Gray, T. S., Carney, M. E., & Magnuson, D. J. (2008) · Neuroendocrinology · doi:10.1159/000125260 · Cited by 331 · see citing works
Localization and Regulation of Glucocorticoid and Mineralocorticoid Receptor Messenger RNAs in the Hippocampal Formation of the Rat
Herman, J. P., Patel, P. D., Akil, H., & Watson, S. J. (1989) · Molecular Endocrinology · doi:10.1210/mend-3-11-1886 · Cited by 328 · see citing works
Self-citation
Anatomical resolution of two types of corticosterone receptor sites in rat brain with in vitro autoradiography and computerized image analysis
Reul, J. M. H. M., & de Kloet, E. R. (1986) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(86)90063-4 · Cited by 325 · see citing works
Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala
Dayas, C. V., Buller, K. M., & Day, T. A. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00645.x · Cited by 303 · see citing works
Hypothalamic-Pituitary-Adrenal Response to Chronic Stress in Five Inbred Rat Strains: Differential Responses Are Mainly Located at the Adrenocortical Level
Gómez-Oliver, F., Lahmame, A., de Kloet, E. R., & Armario, A. (2008) · Neuroendocrinology · doi:10.1159/000126973 · Cited by 264 · see citing works
Chronic social stress alters levels of corticotropin-releasing factor and arginine vasopressin mRNA in rat brain
Albeck, D. S., McKittrick, C. R., Blanchard, D. C., Blanchard, R. J., Nikulina, J., McEwen, B. S., & Sakai, R. R. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-12-04895.1997 · Cited by 261 · see citing works
Adaptation in patterns of c‐fos expression in the brain associated with exposure to either single or repeated social stress in male rats
Martı́nez, M., Phillips, P. J., & Herbert, J. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00011.x · Cited by 253 · see citing works
The medial prefrontal cortex differentially regulates stress‐induced c‐fos expression in the forebrain depending on type of stressor
Figueiredo, H. F., Bruestle, A., Bodie, B., Dolgas, C. M., & Herman, J. P. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02932.x · Cited by 251 · see citing works
Self-citation
Stress Integration after Acute and Chronic Predator Stress: Differential Activation of Central Stress Circuitry and Sensitization of the Hypothalamo-Pituitary-Adrenocortical Axis
Figueiredo, H. F., Bodie, B., Tauchi, M., Dolgas, C. M., & Herman, J. P. (2003) · Endocrinology · doi:10.1210/en.2003-0713 · Cited by 245 · see citing works
Self-citation
Role of the ventral subiculum in stress integration
Herman, J. P., & Mueller, N. K. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.05.035 · Cited by 235 · see citing works
Self-citation
Topographic patterns of brain activity in response to swim stress: assessment by 2-deoxyglucose uptake and expression of Fos-like immunoreactivity
Duncan, G. E., Johnson, K., & Breese, G. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03932.1993 · Cited by 223 · see citing works
Contribution of the Ventral Subiculum to Inhibitory Regulation of the Hypothalamo‐Pituitary‐Adrenocortical Axis
Herman, J. P., Cullinan, W. E., Morano, M. I., Akil, H., & Watson, S. J. (1995) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1995.tb00784.x · Cited by 214 · see citing works
Self-citation
Anatomical interactions between the central amygdaloid nucleus and the hypothalamic paraventricular nucleus of the rat: a dual tract-tracing analysis
Prewitt, C. M., & Herman, J. P. (1998) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(98)00045-3 · Cited by 205 · see citing works
Self-citation
Ventral subiculum regulates hypothalamo–pituitary–adrenocortical and behavioural responses to cognitive stressors
Herman, J. P., Dolgas, C. M., & Carlson, S. L. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00055-4 · Cited by 193 · see citing works
Self-citation
Differential forebrain c-fos mRNA induction by ether inhalation and novelty: evidence for distinctive stress pathways
Emmert, M. H., & Herman, J. P. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01931-9 · Cited by 170 · see citing works
Self-citation
Feedback and facilitation in the adrenocortical system: unmasking facilitation by partial inhibition of the glucocorticoid response to prior stress
Akana, S. F., Dallman, M. F., BRADBURY, M. J., Scribner, K. A., Strack, A. M., & Walker, C. D. (1992) · Endocrinology · doi:10.1210/endo.131.1.1319329 · Cited by 168 · see citing works
Hypoactivity of the Hypothalamo-Pituitary-Adrenocortical Axis during Recovery from Chronic Variable Stress
Ostrander, M. M., Ulrich‐Lai, Y. M., Choi, D. C., Richtand, N. M., & Herman, J. P. (2006) · Endocrinology · doi:10.1210/en.2005-1041 · Cited by 168 · see citing works
Self-citation
Excitatory Influence of the Locus Coeruleus in Hypothalamic‐Pituitary‐Adrenocortical Axis Responses to Stress
Ziegler, Cass, & Herman, J. P. (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00337.x · Cited by 162 · see citing works
Self-citation
Differential effect of amygdaloid lesions on CRF-41, ACTH and corticosterone responses following neural stimuli
Feldman, S., Conforti, N., Itzik, A., & Weidenfeld, J. (1994) · Brain Research · doi:10.1016/s0006-8993(09)90005-1 · Cited by 153 · see citing works
Limbic and HPA axis function in an animal model of chronic neuropathic pain
Ulrich-Lai, Y. M., Xie, W., Meij, J. T. A., Dolgas, C. M., Yu, L., & Herman, J. P. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.03.012 · Cited by 146 · see citing works
Self-citation
Enhanced nucleus accumbens dopamine and plasma corticosterone stress responses in adult rats with neonatal excitotoxic lesions to the medial prefrontal cortex
Brake, W. G., Flores, G., Francis, D. D., Meaney, M. J., Srivastava, L. K., & Gratton, A. P. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00002-6 · Cited by 138 · see citing works
The central amygdala modulates hypothalamic–pituitary–adrenal axis responses to systemic interleukin-1β administration
Xu, Y., Day, T. A., & Buller, K. M. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00311-5 · Cited by 126 · see citing works
The preoptic area and bed nucleus of the stria terminalis are involved in the effects of the amygdala on adrenocortical secretion
Feldman, S., Conforti, N., & Saphier, D. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90107-f · Cited by 125 · see citing works
Adrenocortical Response to Stress in Rats with Lesions in Hippocampus and Amygdala.
Knigge, K. M. (1961) · Experimental Biology and Medicine · doi:10.3181/00379727-108-26832 · Cited by 120 · see citing works
Differential Expression of c‐fos mRNA Within Neurocircuits of Male Hamsters Exposed to Acute or Chronic Defeat
Kollack‐Walker, Don, Watson, & Akil (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00354.x · Cited by 113 · see citing works
Glucocorticoid Negative Feedback and Glucocorticoid Receptors After Hippocampectomy in Rats
Magariños, A., Somoza, G., & De Nicola, A. (1987) · Hormone and Metabolic Research · doi:10.1055/s-2007-1011753 · Cited by 110 · see citing works
Sensitivity to glucocorticoid-mediated fast-feedback regulation of the hypothalamic–pituitary–adrenal axis is dependent upon stressor specific neurocircuitry
Thrivikraman, K. V., Nemeroff, C. B., & Plotsky, P. M. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02405-7 · Cited by 105 · see citing works
A Comparison of the Pituitary Adrenal Activity Elicited by Electrical Stimulation of Preoptic, Amygdaloid and Hypothalamic Sites in the Rat Brain
Redgate, E. S., & Fahringer, E. E. (2008) · Neuroendocrinology · doi:10.1159/000122182 · Cited by 98 · see citing works
Glucocorticoid receptor antagonists in the hippocampus modify the negative feedback following neural stimuli
Feldman, S., & Weidenfeld, J. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01054-9 · Cited by 95 · see citing works
Regulation of Chronic Stress‐Induced Changes in Hypothalamic‐Pituitary‐Adrenal Activity by the Basolateral Amygdala
Bhatnagar, S., VINING, C., & DENSKI, K. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1314.050 · Cited by 93 · see citing works
Differential fornix ablations and the circadian rhythmicity of adrenal corticosteroid secretion
Fischette, C. T., Komisaruk, B. R., Edinger, H. M., Feder, H. H., & Siegel, A. (1980) · Brain Research · doi:10.1016/0006-8993(80)90073-6 · Cited by 89 · see citing works
Plasma 17-hydroxycorticosteroid levels during electrical stimulation of the amygdaloid complex in conscious monkeys
Mason, J. W. (1958) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1958.196.1.44 · Cited by 85 · see citing works
Stressor-Selective Role of the Ventral Subiculum in Regulation of Neuroendocrine Stress Responses
Mueller, N. K., Dolgas, C. M., & Herman, J. P. (2004) · Endocrinology · doi:10.1210/en.2004-0097 · Cited by 81 · see citing works
Self-citation
Hypothalamo-Pituitary-Adrenocortical Regulation Following Lesions of the Central Nucleus of the Amygdala
Prewitt, C. M. F., & Herman, J. P. (1997) · Stress · doi:10.3109/10253899709013746 · Cited by 80 · see citing works
Self-citation
Chronic stress enhances vasopressin but not corticotropin-releasing factor secretion during hypoglycemia
de Goeij, D. C. E., Binnekade, R., & Tilders, F. J. H. (1992) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1992.263.2.e394 · Cited by 74 · see citing works
The effect of hippocampal lesion on pituitary-adrenal function.
FENDLER, K., Karmos, G., & Telegdy, G. (1961) · PubMed · Cited by 72 · see citing works
Patterns of Fos-Immunoreactivity in the CNS Induced by Repeated Hemorrhage in Conscious Rats: Correlations with Pituitary-Adrenal Axis Activity
Thrivikraman, K. V., Su, Y., & Plotsky, P. M. (1997) · Stress · doi:10.3109/10253899709014745 · Cited by 70 · see citing works
Elevation of Hypophysial Portal Concentrations of Adrenocorticotropin Secretagogues after Fornix Transection*
Sapolsky, R. M., Armanini, M. P., Sutton, S. W., & Plotsky, P. M. (1989) · Endocrinology · doi:10.1210/endo-125-6-2881 · Cited by 66 · see citing works
Effect of Electrical Stimulation of the Hippocampus Upon Corticosteroid Levels in the Freely-Behaving, Non-Stressed Rat
Casady, R. L., & Taylor, A. N. (2008) · Neuroendocrinology · doi:10.1159/000122470 · Cited by 66 · see citing works
Presynaptic alterations associated with enhancement of evoked release and synthesis of norepinephrine in hippocampus of chronically cold-stressed rats
Nisenbaum, L. K., & Abercrombie, E. D. (1993) · Brain Research · doi:10.1016/0006-8993(93)91469-9 · Cited by 60 · see citing works
Amygdalectomy Inhibits Adrenocortical Responses to Somatosensory and Olfactory Stimulation
Feldman, S., & Conforti, N. (2008) · Neuroendocrinology · doi:10.1159/000123182 · Cited by 59 · see citing works
Effects of cortisol implants in the brainstem and ventral hippocampus on diurnal corticosteroid levels
Slusher, M. A. (1966) · Experimental Brain Research · doi:10.1007/bf00236870 · Cited by 58 · see citing works
The effect of electrical stimulation of medial temporal lobe structures in epileptic patients upon ACTH, prolactin, and growth hormone
Gallagher, B. B., Flanigin, H. F., King, D. W., & Littleton, W. (1987) · Neurology · doi:10.1212/wnl.37.2.299 · Cited by 51 · see citing works
Medial prefrontal cortex suppression of the hypothalamic–pituitary–adrenal axis response to a physical stressor, systemic delivery of interleukin‐1β
Crane, J. W., Ebner, K., & Day, T. A. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02568.x · Cited by 43 · see citing works
Increased stress vulnerability after a prefrontal cortex lesion in female rats
Gerrits, M., Westenbroek, C., Fokkema, D. S., Jongsma, M. E., den Boer, J. A., & Horst, G. J. T. (2003) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2003.08.004 · Cited by 39 · see citing works

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Voorhees, J. L., Tarr, A. J., Wohleb, E. S., Godbout, J. P., Mo, X., Sheridan, J. F., Eubank, T. D., & Marsh, C. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058488 · Cited by 236 · see citing works
Hypothalamic and other connections with dorsal CA2 area of the mouse hippocampus
Cui, Z., Gerfen, C. R., & Young, W. S. (2013) · Journal of Comparative Neurology · doi:10.1002/cne.23263 · Cited by 214 · see citing works
5-HT1A receptors on mature dentate gyrus granule cells are critical for the antidepressant response
Samuels, B. A., Anacker, C., Hu, A., Levinstein, M. R., Pickenhagen, A., Tsetsenis, T., Madroñal, N., Donaldson, Z. R., Drew, L. J., Dranovsky, A., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4116 · Cited by 200 · see citing works
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Roy, B., Dunbar, M., Shelton, R. C., & Dwivedi, Y. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.175 · Cited by 199 · see citing works
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Anacker, C., Scholz, J., O’Donnell, K. J., Allemang-Grand, R., Diorio, J., Bagot, R. C., Nestler, E. J., Hen, R., Lerch, J. P., & Meaney, M. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.009 · Cited by 167 · see citing works
Impact of early adversity on glucocorticoid regulation and later mental disorders
Strüber, N., Strüber, D., & Roth, G. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.10.015 · Cited by 173 · see citing works
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Myers, B., McKlveen, J. M., & Herman, J. P. (2012) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-012-9801-y · Cited by 175 · see citing works
“The GR is densely expressed in the PVN as well as numerous brain regions implicated in HPA axis regulation, all of which may contribute to feedback regulation (Reul and de Kloet 1985; de Kloet and Reul 1987; Jankord and Herman 2008).”
Self-citation
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Marques, A. H., Bjørke-Monsen, A.-L., Teixeira, A. L., & Silverman, M. N. (2015) · Brain Research · doi:10.1016/j.brainres.2014.10.051 · Cited by 166 · see citing works
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Arloth, J., Bogdan, R., Weber, P., Frishman, G., Menke, A., Wagner, K. V., Balsevich, G., Schmidt, M. V., Karbalai, N., Czamara, D., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.034 · Cited by 142 · see citing works
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Lopez, M. F., Doremus-Fitzwater, T. L., & Becker, H. C. (2011) · Alcohol · doi:10.1016/j.alcohol.2010.08.017 · Cited by 146 · see citing works
Oxidative and nitrosative stress pathways in the brain of socially isolated adult male rats demonstrating depressive- and anxiety-like symptoms
Filipović, D., Todorović, N., Bernardi, R. E., & Gass, P. (2017) · Brain Structure and Function · doi:10.1007/s00429-016-1218-9 · Cited by 138 · see citing works
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Kim, S.-J., Lee, H., Lee, G., Oh, S.-J., Shin, M.-K., Shim, I., & Bae, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042054 · Cited by 130 · see citing works
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Buchanan, T. W., Driscoll, D., Mowrer, S. M., Sollers, J. J., Thayer, J. F., Kirschbaum, C., & Tranel, D. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.09.006 · Cited by 128 · see citing works
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Maras, P. M., Molet, J., Chen, Y., Rice, C., Ji, S. G., Solodkin, A., & Baram, T. Z. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.12 · Cited by 118 · see citing works
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Zhu, L.-J., Liu, M.-Y., Li, H., Liu, X., Chen, C., Han, Z., Wu, H.-Y., Jing, X., Zhou, H.-H., Suh, H., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097689 · Cited by 114 · see citing works
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Sarabdjitsingh, R. A., Conway-Campbell, B. L., Leggett, J. D., Waite, E. J., Meijer, O. C., de Kloet, E. R., & Lightman, S. L. (2010) · Endocrinology · doi:10.1210/en.2010-0832 · Cited by 116 · see citing works
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Lodge, D. J., & Grace, A. A. (2011) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2010.08.002 · Cited by 109 · see citing works
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Ganon-Elazar, E., & Akirav, I. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.01.014 · Cited by 98 · see citing works
Children under stress–COMT genotype and stressful life events predict cortisol increase in an acute social stress paradigm
Armbruster, D., Mueller, A., Strobel, A., Lesch, K.-P., Brocke, B., & Kirschbaum, C. (2012) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145711001763 · Cited by 87 · see citing works
Stress-induced alterations in anxiety-like behavior and adaptations in plasticity in the bed nucleus of the stria terminalis
Conrad, K. L., Louderback, K. M., Gessner, C. P., & Winder, D. G. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.03.001 · Cited by 71 · see citing works
One left dorsolateral prefrontal cortical HF-rTMS session attenuates HPA-system sensitivity to critical feedback in healthy females
Baeken, C., Vanderhasselt, M. A., Remue, J., Rossi, V., Schiettecatte, J., Anckaert, E., & De Raedt, R. (2014) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2014.02.019 · Cited by 63 · see citing works
Glutamate receptors in domestication and modern human evolution
O’Rourke, T., & Boeckx, C. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.10.004 · Cited by 50 · see citing works
Maternal separation changes maternal care, anxiety-like behaviour and expression of paraventricular oxytocin and corticotrophin-releasing factor immunoreactivity in lactating rats
Baracz, S. J., Everett, N. A., Robinson, K. J., Campbell, G. R., & Cornish, J. L. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12861 · Cited by 46 · see citing works
Lifetime modulation of the pain system via neuroimmune and neuroendocrine interactions
Zouikr, I., & Karshikoff, B. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00276 · Cited by 45 · see citing works
The Gut Microbiota’s Role in Neurological, Psychiatric, and Neurodevelopmental Disorders
Charitos, I. A., Inchingolo, A. M., Ferrante, L., Inchingolo, F., Inchingolo, A. D., Castellaneta, F., Cotoia, A., Palermo, A., Scacco, S., & Dipalma, G. (2024) · Nutrients · doi:10.3390/nu16244404 · Cited by 44 · see citing works
An immune gate of depression—Early neuroimmune development in the formation of the underlying depressive disorder
Kowalczyk, M., Szemraj, J., Bliźniewska, K., Maes, M., Berk, M., Su, K.-P., & Gałecki, P. (2019) · Pharmacological Reports · doi:10.1016/j.pharep.2019.05.022 · Cited by 38 · see citing works
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Jimenez, V. A., Herman, M. A., Cuzon Carlson, V. C., Walter, N. A., Grant, K. A., & Roberto, M. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-018-0290-7 · Cited by 29 · see citing works
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Gałecka, M., Bliźniewska-Kowalska, K., Maes, M., Su, K.-P., & Gałecki, P. (2021) · Pharmacological Reports · doi:10.1007/s43440-020-00202-2 · Cited by 27 · see citing works
Association of amygdala volumes with cortisol secretion in unipolar depressed patients
Schuhmacher, A., Mössner, R., Jessen, F., Scheef, L., Block, W., Belloche, A. C., Lennertz, L., Welper, H., Höfels, S., Pfeiffer, U., et al. (2012) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2011.09.007 · Cited by 25 · see citing works
Exposure of mother rats to chronic unpredictable stress before pregnancy alters the metabolism of gamma-aminobutyric acid and glutamate in the right hippocampus of offspring in early adolescence in a sexually dimorphic manner
Huang, Y., Shen, Z., Hu, L., Xia, F., Li, Y., Zhuang, J., Chen, P., & Huang, Q. (2016) · Psychiatry Research · doi:10.1016/j.psychres.2016.10.005 · Cited by 22 · see citing works
Understanding the Neuroepigenetic Constituents of Suicide Brain
Roy, B., & Dwivedi, Y. (2018) · Progress in Molecular Biology and Translational Science · doi:10.1016/bs.pmbts.2018.01.007 · Cited by 17 · see citing works
Site-specific changes in brain extra-SCN oscillators during early pregnancy in the rat
Schrader, J. A., Nunez, A. A., & Smale, L. (2011) · Journal of Biological Rhythms · doi:10.1177/0748730411409714 · Cited by 12 · see citing works

Authors: Jankord, R., & Herman, J. P.
Affiliations: University of Cincinnati (US)
Corresponding author: Jankord, Ryan
ORCID: Jankord, Ryan
Herman, James P.
Venue: Annals of the New York Academy of Sciences
Publisher: Wiley
Published: 2008-12
Volume: 1148
Issue: 1
Pages: 64-73
ISSN: 0077-8923 (ISSN-L)
1749-6632
DOI: 10.1196/annals.1410.012
PMC: PMC2637449
OpenAlex: W2051831861
Cited by: 578
References: 70
Citations by year: 2026: 17 · 2025: 20 · 2024: 40 · 2023: 34 · 2022: 38 · 2021: 35 · 2020: 42 · 2019: 34 · 2018: 25 · 2017: 34 · 2016: 33 · 2015: 33 · 2014: 33 · 2013: 37 · 2012: 51
FWCI: 1.68
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 10 d)
Locations: Annals of the New York Academy of Sciences (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute on Aging (AG12962, R01AG012962)
National Institute of Mental Health (R01MH049698, MH 069725, MH049698, MH 069680, R01MH069725)
National Institute of Diabetes and Digestive and Kidney Diseases (DK-059803, T32DK059803)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords: hypothalamic-pituitary-adrenal axis, limbic system, paraventricular nucleus, acute stress, chronic stress, glucocorticoid stress response, neurocircuitry, HPA axis hyperactivity
MeSH terms: Amygdala, Animals, Cerebral Cortex, Glucocorticoids, Hippocampus, Humans, Hypothalamo-Hypophyseal System, Limbic System, Pituitary-Adrenal System, Stress, Physiological

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Limbic Regulation of Hypothalamo‐Pituitary‐Adrenocortical Function during Acute and Chronic Stress

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