Gender and puberty interact on the stress-induced activation of parvocellular neurosecretory neurons and corticotropin-releasing hormone messenger ribonucleic acid expression in the rat

Viau, Victor; Bingham, Brenda; Davis, Jennifer; Lee, Patricia; Wong, Margaret

doi:10.1210/en.2004-0846

Cited by 266Stress Responses and CortisolHypothalamic control of reproductive hormonesNeuroendocrine regulation and behavior

Gender and puberty interact on the stress-induced activation of parvocellular neurosecretory neurons and corticotropin-releasing hormone messenger ribonucleic acid expression in the rat

Viau, Victor, Bingham, Brenda, Davis, Jennifer, Lee, Patricia, Wong, Margaret·2005·Endocrinology

DOI 10.1210/en.2004-0846

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Abstract

Individual variations in hypothalamic-pituitary-adrenal (HPA) function are most evident at or beyond the time of puberty, when marked changes in sex steroid release occur. To explore the nature by which gender differences in HPA function emerge we examined in prepubertal (∼30-d-old) and postpubertal (∼60-d-old) male and female rats HPA activity under basal conditions and in response to 30 min of restraint. Within the ACTH-regulating, medial parvocellular portion of the paraventricular nucleus, restraint-induced Fos protein and arginine vasopressin heteronuclear RNA were lower in 60- than in 30-d-old males. No such age-related shift in the response of these synaptic and transcriptional markers of cellular activation occurred in female rats. Basal CRH mRNA expression levels in the paraventricular nucleus increased with age in female but not male rats. Conversely, only male rats showed an age-related increase in basal CRH mRNA in the central amygdala, suggesting that neuronal and neurosecretory CRH-expressing cell types are subject to different pubertal and gender influences. We conclude that gonadal regulation of the HPA axis develops via distinct mechanisms in males and females. Puberty-related shifts in parvocellular neurosecretory function in males are emphasized by stress-induced shifts in neuronal activation, whereas biosynthetic alterations dominate in female rats.

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Sex-dependent patterns are observed in the activation of PVN neurons that control HPA axis reactivity after stress.
“Furthermore, these sex-dependent patterns are also observed in the activation of PVN neurons controlling HPA axis reactivity following stress (Larkin, Binks, Li, & Selvage, 2010; Seale, Wood, Atkinson, Harbuz, & Lightman, 2004; Viau, Bingham, Davis, Lee, & Wong, 2005).”
From Hypothalamic–pituitary–adrenal and hypothalamic–pituitary–gonadal axes: sex differences in regulation of stress responsivity (2017) · cites this paper as Viau, Bingham, Davis, Lee, & Wong, 2005
Androgens and estrogen modulate cortisol synthesis in the adrenal cortex and CRH and AVP synthesis in the hypothalamus, with the latter effect mediated by sex hormone receptors in the amygdala.
“Androgens and estrogen modulate cortisol synthesis in the adrenal cortex and CRH and AVP synthesis in the hypothalamus; the latter effect is mediated by sex hormone receptors in the amygdala (Viau, 2002; Viau et al., 2005)”
From The Adaptive Calibration Model of stress responsivity (2011) · cites this paper as Viau et al., 2005

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Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
Estimation of nuclear population from microtome sections
Abercrombie, M. (1946) · The Anatomical Record · doi:10.1002/ar.1090940210 · Cited by 4,363 · see citing works
Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo–pituitary–adrenocortical responsiveness
Herman, J. P., Figueiredo, H., Mueller, N. K., Ulrich-Lai, Y., Ostrander, M. M., Choi, D. C., & Cullinan, W. E. (2003) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2003.07.001 · Cited by 1,586 · see citing works
A Complete Protocol for In Situ Hybridization of Messenger RNAs in Brain and Other Tissues With Radio-labeled Single-Stranded RNA Probes
Simmons, D. M., Arriza, J. L., & Swanson, L. W. (1989) · Journal of Histotechnology · doi:10.1179/his.1989.12.3.169 · Cited by 920 · see citing works
Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety
Walker, D. L., Toufexis, D. J., & Davis, M. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01282-2 · Cited by 838 · see citing works
Functional Cross‐Talk Between the Hypothalamic‐Pituitary‐Gonadal and ‐Adrenal Axes
Viau, V. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2002.00798.x · Cited by 744 · see citing works
Self-citation
Changes with Age in Levels of Serum Gonadotropins, Prolactin, and Gonadal Steroids in Prepubertal Male and Female Rats
DÖHLER, K.-D., & Wuttke, W. (1975) · Endocrinology · doi:10.1210/endo-97-4-898 · Cited by 729 · see citing works
Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat
VIAU, V., & MEANEY, M. J. (1991) · Endocrinology · doi:10.1210/endo-129-5-2503 · Cited by 666 · see citing works
Self-citation
Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system
Whitnall, M. H. (1993) · Progress in Neurobiology · doi:10.1016/0301-0082(93)90035-q · Cited by 582 · see citing works
Are adolescents the victims of raging hormones: evidence for activational effects of hormones on moods and behavior at adolescence
Buchanan, C. M., Eccles, J. S., & Becker, J. B. (1992) · Psychological Bulletin · doi:10.1037/0033-2909.111.1.62 · Cited by 572 · see citing works
Stress and Plasticity in the Limbic System
Sapolsky, R. M. (2003) · Neurochemical Research · doi:10.1023/a:1026021307833 · Cited by 489 · see citing works
Pediatric Stress: Hormonal Mediators and Human Development
Charmandari, E., Kino, T., Souvatzoglou, E., & Chrousos, G. P. (2003) · Hormone Research in Paediatrics · doi:10.1159/000069325 · Cited by 364 · see citing works
Dopamine: a key regulator to adapt action, emotion, motivation and cognition
Nieoullon, A., & Coquerel, A. (2003) · Current Opinion in Neurology · doi:10.1097/00019052-200312002-00002 · Cited by 315 · see citing works
Sequence of stress-induced alterations in indices of synaptic and transcriptional activation in parvocellular neurosecretory neurons
Kovacs, K., & Sawchenko, P. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-01-00262.1996 · Cited by 310 · see citing works
A comparison of two immediate-early genes, c-fos and NGFI-B, as markers for functional activation in stress-related neuroendocrine circuitry
Chan, R., Brown, E., Ericsson, A., Kovacs, K., & Sawchenko, P. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-12-05126.1993 · Cited by 289 · see citing works
Neuroadaptive mechanisms of addiction: studies on the extended amygdala
Koob, G. F. (2003) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2003.08.005 · Cited by 278 · see citing works
Stress and the developing limbic-hypothalamic-pituitary-adrenal axis
M. Vázquez, D. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00029-8 · Cited by 274 · see citing works
Neurotransmitter Regulation of Cellular Activation and Neuropeptide Gene Expression in the Paraventricular Nucleus of the Hypothalamus
Cole, R. L., & Sawchenko, P. E. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-00959.2002 · Cited by 253 · see citing works
Sex Differences in Chronic Stress Effects on Memory in Rats
Luine, V. (2002) · Stress · doi:10.1080/1025389021000010549 · Cited by 250 · see citing works
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Figueiredo, H. F., Dolgas, C. M., & Herman, J. P. (2002) · Endocrinology · doi:10.1210/endo.143.7.8888 · Cited by 237 · see citing works
Puberty: a period of both organizational and activational effects of steroid hormones on neurobehavioural development
Romeo, R. D. (2003) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2003.01106.x · Cited by 233 · see citing works
Salivary cortisol and dehydroepiandrosterone in relation to puberty and gender
Netherton, C. M., Goodyer, I. M., Tamplin, A., & Herbert, J. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(02)00150-6 · Cited by 231 · see citing works
Postweaning Development of Negative Feedback in the Pituitary-Adrenal System of the Rat
Goldman, L., Winget, C., Hollingshead, G. W., & Levine, S. D. (2008) · Neuroendocrinology · doi:10.1159/000122169 · Cited by 202 · see citing works
Testosterone Cannot Activate an Adult-Like Stress Response in Prepubertal Male Rats
Romeo, R. D., Lee, S. H., Chhua, N., McPherson, C. R., & McEwen, B. S. (2004) · Neuroendocrinology · doi:10.1159/000077270 · Cited by 197 · see citing works
Vasopressin and Corticotropin-Releasing Hormone Gene Responses to Novel Stress in Rats Adapted to Repeated Restraint
Ma, X., Lightman, S. L., & Aguilera, G. (1999) · Endocrinology · doi:10.1210/endo.140.8.6943 · Cited by 182 · see citing works
Glucocorticoid Negative Feedback Selectively Targets Vasopressin Transcription in Parvocellular Neurosecretory Neurons
Kovács, K. J., Földes, A., & Sawchenko, P. E. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-10-03843.2000 · Cited by 172 · see citing works
Androgen Inhibits, While Oestrogen Enhances, Restraint‐Induced Activation of Neuropeptide Neurones in the Paraventricular Nucleus of the Hypothalamus
Lund, T. D., Munson, D. J., Haldy, M. E., & Handa, R. J. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.0953-8194.2004.01167.x · Cited by 172 · see citing works
Hypophysiotropic neurons of the paraventricular nucleus respond in spatially, temporally, and phenotypically differentiated manners to acute vs. repeated restraint stress: Rapid publication
Viau, V., & Sawchenko, P. E. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10178 · Cited by 153 · see citing works
Self-citation
Neonatal sex hormones have `organizational' effects on the hypothalamic-pituitary-adrenal axis of male rats
McCormick, C. M., Furey, B. F., Child, M., Sawyer, M. J., & Donohue, S. M. (1998) · Developmental Brain Research · doi:10.1016/s0165-3806(97)00155-7 · Cited by 149 · see citing works
Pituitary-Adrenal Response to Ether Vapor in the Weanling Animal: Characterization of the Inhibitory Effect of Glucocorticoids on Adrenocorticotropin Secretion
Vázquez, D. M., & Akil, H. (1993) · Pediatric Research · doi:10.1203/00006450-199311000-00017 · Cited by 144 · see citing works
The Amygdala, Panic Disorder, and Cardiovascular Responses
Shekhar, A., Sajdyk, T. J., Gehlert, D. R., & Rainnie, D. G. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07090.x · Cited by 137 · see citing works
In SituHybridization Analysis of Arginine Vasopressin Gene Transcription Using Intron-Specific Probes
Herman, J. P., Schäfer, M. K.-H., Watson, S. J., & Sherman, T. G. (1991) · Molecular Endocrinology · doi:10.1210/mend-5-10-1447 · Cited by 136 · see citing works
Corticotropin releasing hormone mRNA is elevated on the afternoon of proestrus in the parvocellular paraventricular nuclei of the female rat
BOHLER, H. C. L., Zoeller, R. T., King, J. C., Rubin, B. S., Weber, R. F. A., & Merriam, G. R. (1990) · Molecular Brain Research · doi:10.1016/0169-328x(90)90025-9 · Cited by 136 · see citing works
Diurnal Variations in the Content of Preprocorticotropin-Releasing Hormone Messenger Ribonucleic Acids in the Hypothalamic Paraventricular Nucleus of Rats of Both Sexes as Measured by in Situ Hybridization*
WATTS, A. G., & Swanson, L. W. (1989) · Endocrinology · doi:10.1210/endo-125-3-1734 · Cited by 110 · see citing works
Sex differences in adrenocortical structure and function
Majchrzak, M., & Malendowicz, L. K. (1983) · Cell and Tissue Research · doi:10.1007/bf00213800 · Cited by 103 · see citing works
Androgens Alter Corticotropin Releasing Hormone and Arginine Vasopressin mRNA Within Forebrain Sites Known to Regulate Activity in the Hypothalamic‐Pituitary‐Adrenal Axis
Viau, V., Soriano, L., & Dallman, M. F. (2001) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2001.00653.x · Cited by 97 · see citing works
Self-citation
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CHIAPPA, S. A., & Fink, G. (1977) · Journal of Endocrinology · doi:10.1677/joe.0.0720211 · Cited by 97 · see citing works
Androgen-Sensitive Changes in Regulation of Restraint-Induced Adrenocorticotropin Secretion between Early and Late Puberty in Male Rats
Gómez-Oliver, F., Manalo, S. L., & Dallman, M. F. (2003) · Endocrinology · doi:10.1210/en.2003-0565 · Cited by 91 · see citing works
Stress and reproduction in domestic animals
LIPTRAP, R. M. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb49941.x · Cited by 90 · see citing works
Marked Regulatory Shifts in Gonadal, Adrenal, and Metabolic System Responses to Repeated Restraint Stress Occur within a 3-Week Period in Pubertal Male Rats
Gómez-Oliver, F., Houshyar, H., & Dallman, M. F. (2002) · Endocrinology · doi:10.1210/endo.143.8.8929 · Cited by 88 · see citing works
The Neurobiology of Stress: Understanding Regulation of Affect During Female Biological Transitions
Dorn, L. D., & Chrousos, G. (1997) · Seminars in Reproductive Medicine · doi:10.1055/s-2008-1067965 · Cited by 76 · see citing works
Influence of the Estrous Cycle on c-fos and CRH Gene Transcription in the Brain of Endotoxin-Challenged Female Rats
Nappi, R. E., Bonneau, M.-J., & Rivest, S. (2008) · Neuroendocrinology · doi:10.1159/000127162 · Cited by 64 · see citing works
A Testicular Influence on Restraint-Induced Activation of Medial Parvocellular Neurons in the Paraventricular Nucleus in the Male Rat
Viau, V., Lee, P. J., Sampson, J., & Wu, J. (2003) · Endocrinology · doi:10.1210/en.2003-0064 · Cited by 64 · see citing works
Self-citation
Minireview: Adrenal-gonadal interactions at puberty
Ramaley, J. A. (1974) · Life Sciences · doi:10.1016/0024-3205(74)90264-1 · Cited by 58 · see citing works
Diurnal Variation in Plasma Testosterone of the Male Laboratory Rat
Kinson, G. A., & Liu, C.-C. (1973) · Hormone and Metabolic Research · doi:10.1055/s-0028-1096740 · Cited by 55 · see citing works
Preautonomic neurons in the paraventricular nucleus of the hypothalamus contain estrogen receptor β
Stern, J. E., & Zhang, W. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02594-0 · Cited by 53 · see citing works
The development of sex differences in the adrenal morphology and responsiveness in stress of rats from birth to the end of life
Senčar-Čupović, I., & MILKOVIĆ, S. (1976) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(76)90002-6 · Cited by 47 · see citing works
Daily Variation of Plasma Testosterone, Androstenedione, and Corticosterone in Rats under Food Restriction
Leal, A. M. O., & Moreira, A. C. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1321 · Cited by 38 · see citing works
α1 Adrenoreceptors Mediate The Stimulatory Effects of Oestrogen On Stress‐Related Hypothalamic‐Pituitary‐Adrenal Activity in The Female Rat
Viau, V., & Meaney, M. J. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2004.01122.x · Cited by 33 · see citing works
Self-citation
Manipulation of androgens causes different energetic responses to cold in 60- and 40-day-old male rats
Gómez-Oliver, F., & Dallman, M. F. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.280.1.r262 · Cited by 27 · see citing works
Physiological and Behavioral Aspects of Stress in Adolescence
Susman, E. J., Nottelmann, E. D., Dorn, L. D., Inoff‐Germain, G., & Chrousos, G. P. (1988) · Advances in experimental medicine and biology · doi:10.1007/978-1-4899-2064-5_27 · Cited by 22 · see citing works
Neuroendocrine mechanisms in reproductive physiology
Wuttke, W. (1976) · Reviews of physiology, biochemistry and pharmacology · doi:10.1007/bfb0027687 · Cited by 22 · see citing works
ROLE OF TESTOSTERONE IN THE SEXUAL DIMORPHISM OF ADRENAL ACTIVITY AT PUBERTY IN THE GUINEA-PIG
Hani, A. E., Dalle, M., & Delost, P. (1980) · Journal of Endocrinology · doi:10.1677/joe.0.0870455 · Cited by 21 · see citing works
Update on pubertal development
Rieder, J., & Coupey, S. M. (1999) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-199910000-00007 · Cited by 21 · see citing works
PUBERTAL MANIFESTATION OF SEX DIFFERENCE IN CIRCADIAN RHYTHM OF CORTICOTROPHIN-RELEASING ACTIVITY IN THE RAT HYPOTHALAMUS
Honma, S., & Hiroshige, T. (1977) · European Journal of Endocrinology · doi:10.1530/acta.0.0860225 · Cited by 19 · see citing works
The adrenal rhythm and puberty onset in the female rat
Ramaley, J. A. (1978) · Life Sciences · doi:10.1016/0024-3205(78)90181-9 · Cited by 18 · see citing works
Editorial: Stressing the Importance of Sex
Levine, J. E. (2002) · Endocrinology · doi:10.1210/en.2002-221041 · Cited by 18 · see citing works
The Security Circuit: A Proposed Construct for the Central Nervous System
Halpern, G. J., & O'connell, B. E. (2000) · International Journal of Neuroscience · doi:10.3109/00207450008986499 · Cited by 5 · see citing works

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Dallman MF, Viau V, Bhatnagar S, Gomez F, Laugero K, Bell ME 2002 Corticotropin-releasing factor (CRF), corticosteroids, stress and sugar: energy balance, the brain and behavior. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, eds. Hormones, brain, and behavior. New York: Academic Press; 571-632

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“…RNA in the PVN is higher prepubertally in males (Romeo et al., 007; Viau et al., 2005); lower baseline corticosterone and CRH RNA in prepubertal females (Viau et al., 2005); greater expresion of adrenal melanocortin 2 receptor accessory protein mRNA n prepubertal males (Romeo et al., 2014)).”
Influential
Adolescent development, hypothalamic-pituitary-adrenal function, and programming of adult learning and memory
McCormick, C. M., & Mathews, I. Z. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.09.019 · Cited by 230 · see citing works
Gender differences in corticotropin and corticosterone secretion and corticotropin-releasing factor mRNA expression in the paraventricular nucleus of the hypothalamus and the central nucleus of the amygdala in response to footshock stress or psychological stress in rats
Iwasaki-Sekino, A., Mano‐Otagiri, A., Ohata, H., Yamauchi, N., & Shibasaki, T. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.09.003 · Cited by 222 · see citing works
Stress exposure, food intake and emotional state.
Ulrich‐Lai, Y. M., Fulton, S., Wilson, M., Petrovich, G. D., & Rinaman, L. (2015) · PubMed · doi:10.3109/10253890.2015.1062981 · Cited by 210 · see citing works
“It is tempting to suggest that these differences may reflect sex differences in HPA axis regulation (Handa et al., 1994; Toufexis & Wilson, 2012; Viau et al., 2005), and in how HPA axis responses are modified by dietary environment.”
Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis
Burke, A. R., & Miczek, K. A. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3369-1 · Cited by 207 · see citing works
“Adolescent males have greater CRF mRNA expression in the PVN, while the opposite was reported in adolescent females (Romeo et al. 2007; Viau et al. 2005).”
Background
An alternate pathway for androgen regulation of brain function: Activation of estrogen receptor beta by the metabolite of dihydrotestosterone, 5α-androstane-3β,17β-diol
Handa, R. J., Pak, T. R., Kudwa, A. E., Lund, T. D., & Hinds, L. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.09.012 · Cited by 205 · see citing works
“Prior to puberty, when testosterone levels are low, the corticosterone response to acute and chronic stress is high relative to the response seen after puberty (Viau et al. 2005, Romeo et al. 2006) which corresponds to elevations in testosterone that occur during the pubertal transition of males.”
Background
Social and non-social anxiety in adolescent and adult rats after repeated restraint
Doremus‐Fitzwater, T. L., Varlinskaya, E. I., & SPEAR, L. P. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.03.025 · Cited by 197 · see citing works
“These findings are in agreement with the previously reported enhancement of acute restraint stress-induced CORT response in adult females relative to their younger counterparts [78], although such age differences among females are not ubiquitous [15].”
Result
Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity
Weintraub, A. Y., Singaravelu, J., & Bhatnagar, S. (2010) · Brain Research · doi:10.1016/j.brainres.2010.04.068 · Cited by 186 · see citing works
Sex differences in stress responses: a critical role for corticotropin-releasing factor
Bangasser, D. A., & Wiersielis, K. (2018) · HORMONES · doi:10.1007/s42000-018-0002-z · Cited by 193 · see citing works
“some to be elevated in the central nucleus of the amygdala in female relative to male rats [95], although this sex difference is not always observed [96].”
Background
The juvenile transition: A developmental switch point in human life history
Giudice, M. D., Angeleri, R., & Manera, V. (2008) · Developmental Review · doi:10.1016/j.dr.2008.09.001 · Cited by 179 · see citing works
Chronic restraint stress in adolescence differentially influences hypothalamic‐pituitary‐adrenal axis function and adult hippocampal neurogenesis in male and female rats
Barha, C. K., Brummelte, S., Lieblich, S. E., & Galea, L. A. M. (2010) · Hippocampus · doi:10.1002/hipo.20829 · Cited by 164 · see citing works
“…adolescent male and female rats show prolonged corticosterone release in response to a stressor compared to adult rats (Romeo et al., 2004a,b; Viau et al., 2005; Romeo and McEwen, 2006) and adolescent male rats do not habituate to chronic stressors unlike adult rats who eventually show a…”
Background
Stress is a principal factor that promotes tobacco use in females
Torres, O. V., & O'Dell, L. E. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.04.005 · Cited by 164 · see citing works
Sex Differences in Molecular and Cellular Substrates of Stress
Bangasser, D. A., & Valentino, R. J. (2012) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-012-9824-4 · Cited by 160 · see citing works
“Specifically, basal (i.e., unstressed) levels of the glucocorticoid, corticosterone, are elevated in female compared to male rats (Kitay 1961; Viau et al. 2005; Weinstock et al. 1998).”
Influential
The transformation of hormonal stress responses throughout puberty and adolescence
Foilb, A. R., Lui, P., & Romeo, R. D. (2011) · Journal of Endocrinology · doi:10.1530/joe-11-0206 · Cited by 154 · see citing works
“…than that on the adult (Goldman et al. 1973), while others have shown greater post-stress activation of the paraventricular nucleus of the hypothalamus, the brain region integral in initiating this hormonal cascade, and in prepubertal compared to adult rats (Viau et al. 2005, Romeo et al. 2006a).”
Background
Sex Differences in Social Interaction Behavior Following Social Defeat Stress in the Monogamous California Mouse (Peromyscus californicus)
Trainor, B. C., Pride, M. C., Villalon Landeros, R., Knoblauch, N. W., Takahashi, E. Y., Silva, A. L., & Crean, K. K. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017405 · Cited by 157 · see citing works
Anxiety and hippocampal neuronal activity: Relationship and potential mechanisms
Ghasemi, M., Navidhamidi, M., Rezaei, F., Azizikia, A., & Mehranfard, N. (2021) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-021-00973-y · Cited by 167 · see citing works
“For example, compared with males, female rodents have greater HPA axis activation and subsequent higher levels of glucocorticoids (Bangasser, 2013; Kitay, 1961; Viau et al., 2005; Weinstock et al., 1998), a state that is thought to cause anxiety.”
Background
A gut feeling: Microbiome-brain-immune interactions modulate social and affective behaviors
Sylvia, K. E., & Demas, G. E. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.02.001 · Cited by 151 · see citing works
“logical stressors, and females show a higher average concentration of glucocorticoids than males (Viau et al., 2005).”
Background
Neurobiology of resilience in depression: immune and vascular insights from human and animal studies
Dudek, K., Dion‐Albert, L., Kaufmann, F. N., Tuck, E., Lebel, M., & Ménard, C. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14547 · Cited by 156 · see citing works
“At baseline, female rodents display a more active HPA axis than their male counterparts, as well as higher circulating levels of corticosterone (Kitay, 1961; Viau et al., 2005; Weinstock et al., 1998).”
Background
Sex differences in activated corticotropin-releasing factor neurons within stress-related neurocircuitry and hypothalamic–pituitary–adrenocortical axis hormones following restraint in rats
Babb, J. A., Masini, C. V., Day, H. E. W., & Campeau, S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.12.051 · Cited by 134 · see citing works
How age, sex and genotype shape the stress response
Novais, A., Monteiro, S., Roque, S., Correia‐Neves, M., & Sousa, N. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.11.004 · Cited by 140 · see citing works
“Higher levels of ACTH were also observed at the peak (not basal levels) in cycling rat females in proestrus compared to estrous and di-estrus (Viau and Meaney, 1991).”
Considering Sex as a Biological Variable in Basic and Clinical Studies: An Endocrine Society Scientific Statement
Bhargava, A., Arnold, A. P., Bangasser, D. A., Denton, K. M., Gupta, A., Hilliard Krause, L. M., Mayer, E. A., McCarthy, M., Miller, W. L., Raznahan, A., et al. (2021) · Endocrine Reviews · doi:10.1210/endrev/bnaa034 · Cited by 130 · see citing works
“In female rats, higher levels of CRF mRNA in the paraventricular nucleus are reported that associate with the estrous cycle (276, 277) and are reviewed elsewhere (274).”
Background
Involvement of the Endocannabinoid System in the Ability of Long-Term Tricyclic Antidepressant Treatment to Suppress Stress-Induced Activation of the Hypothalamic–Pituitary–Adrenal Axis
Hill, M. N., Ho, W. ‐. V., Sinopoli, K. J., Viau, V., Hillard, C. J., & Gorzalka, B. B. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301092 · Cited by 116 · see citing works
“…in this study, the region of interest we analyzed in the mpdPVN here is where all CRH neurosecretory cells are amassed (Viau and Sawchenko, 2002; Viau et al, 2005) suggesting that a suppression of stress-induced activation of CRH neurosecretory cells is likely mediating the effect of…”
BackgroundSelf-citation
Puberty, hormones, and sex differences in alcohol abuse and dependence
Witt, E. D. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.10.013 · Cited by 112 · see citing works
Sex Differences in the Serotonergic Influence on the Hypothalamic-Pituitary-Adrenal Stress Axis
Goel, N., & Bale, T. L. (2010) · Endocrinology · doi:10.1210/en.2009-1180 · Cited by 113 · see citing works
Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor
Romeo, R. D., Karatsoreos, I. N., & McEwen, B. S. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.002 · Cited by 107 · see citing works
Sex differences in stress-related receptors: ″micro″ differences with ″macro″ implications for mood and anxiety disorders
Bangasser, D. A. (2013) · Biology of Sex Differences · doi:10.1186/2042-6410-4-2 · Cited by 108 · see citing works
“One such mechanism is greater CRF expression in the hypothalamus of female compared to male rodents, which can translate into greater HPA axis activation [91-94,197].”
BackgroundInfluential
Social Instability in Adolescence Alters the Central and Peripheral Hypothalamic‐Pituitary‐Adrenal Responses to a Repeated Homotypic Stressor in Male and Female Rats
McCormick, C. M., Merrick, A., Secen, J., & Helmreich, D. L. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01515.x · Cited by 106 · see citing works
Adolescence and the ontogeny of the hormonal stress response in male and female rats and mice
Romeo, R. D., Patel, R., Pham, L., & So, V. M. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.020 · Cited by 102 · see citing works
“Moreover, although basal CRH mRNA in the PVN is slightly higher in pre-adolescent versus adult rats (Romeo et al., 2007b), stress results in elevated CRH expression at both ages (McCormick et al., 2007; Romeo et al., 2007b; Viau et al., 2005).”
Background
Sex differences in the hypothalamic–pituitary–adrenal axis: An obstacle to antidepressant drug development?
Kokras, N., Hodes, G. E., Bangasser, D. A., & Dalla, C. (2019) · British Journal of Pharmacology · doi:10.1111/bph.14710 · Cited by 94 · see citing works
“In the PVN, there are several reports that female rats had greater CRF expression than males (Duncko, Kiss, Skultetyova, Rusnak, & Jezova, 2001; Viau et al., 2005), although this difference was not found in every rat study or with the Crh‐IRES‐Cre::Ai14 (tdTomato) reporter mouse (Sterrenburg et al.”
Background
Sex differences in cortisol response to corticotropin releasing hormone challenge over puberty: Pittsburgh Pediatric Neurobehavioral Studies
Stroud, L. R., Papandonatos, G. D., Williamson, D. E., & Dahl, R. E. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.02.017 · Cited by 98 · see citing works
“Our findings also complement preclinical studies revealing the emergence over adolescence/puberty of increases in female basal corticosterone levels, with corresponding decreases observed among males, as well as of increases in adrenal weight and adrenal corticosterone content among females alone (Critchlow et al., 19…”
BackgroundInfluential
A Role for the Androgen Metabolite, 5α‐Androstane‐3β,17β‐Diol, in Modulating Oestrogen Receptor β‐Mediated Regulation of Hormonal Stress Reactivity
Handa, R. J., Weiser, M. J., & Zuloaga, D. G. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01840.x · Cited by 95 · see citing works
Sex differences: Transcriptional signatures of stress exposure in male and female brains
Brivio, E., Lopez, J. P., & Chen, A. (2020) · Genes, Brain and Behavior · doi:10.1111/gbb.12643 · Cited by 95 · see citing works
Sex-Related Differences in Stimulated Hypothalamic-Pituitary-Adrenal Axis during Induced Gonadal Suppression
Putnam, K. T., Chrousos, G. P., Nieman, L. K., & Rubinow, D. R. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-2525 · Cited by 91 · see citing works
“The differential activation of the HPA axis in male and female rodents is primarily a consequence of differential exposure to testosterone and estradiol (37).”
Background
Epigenetic mechanisms in pubertal brain maturation
Morrison, K. E., Rodgers, A. B., Morgan, C. P., & Bale, T. L. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.11.014 · Cited by 90 · see citing works
“…and baseline corticotropin-releasing factor expression, have been associated with the rapid change in stress responsivity, suggesting that puberty stimulates a wholesale change in the regulation of the HPA axis (Goldman et al., 1973; Lui et al., 2012; Romeo et al., 2005; 2007; Viau et al., 2005).”
Background
Roles for androgens in mediating the sex differences of neuroendocrine and behavioral stress responses
Zuloaga, D. G., Heck, A., Guzman, R. M. D., & Handa, R. J. (2020) · Biology of Sex Differences · doi:10.1186/s13293-020-00319-2 · Cited by 96 · see citing works
Sex Differences in Stress Response: Classical Mechanisms and Beyond
Hodes, G. E., Bangasser, D. A., Sotiropoulos, I., Kokras, N., & Dalla, C. (2023) · Current Neuropharmacology · doi:10.2174/1570159x22666231005090134 · Cited by 95 · see citing works
“For example, stress enhances corticotropin-releasing factor (CRF), ACTH, and corticosterone more in female than male rats [41, 47, 48], but when surgical adrenalectomy is performed in female rats, and corticosterone is substituted, resulting in stable corticosterone levels, females continue to…”
Background
Social control of brain morphology in a eusocial mammal
Holmes, M. M., Rosen, G. J., Jordan, C. L., Vries, G. J. D., Goldman, B. D., & Forger, N. G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610344104 · Cited by 91 · see citing works
Changes in hypothalamic–pituitary–adrenal stress responsiveness before and after puberty in rats
Klein, Z. A., & Romeo, R. D. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.01.012 · Cited by 90 · see citing works
“Moreover, basal expression of CRH in the PVN appears to be higher in male rats prior to puberty (Romeo et al., 2007b), though the opposite trend has been noted in females (Viau et al., 2005).”
Background
Effects of Psychological Stress on Hypertension in Middle-Aged Chinese: A Cross-Sectional Study
Hu, B., Liu, X., Yin, S., Fan, H., Feng, F., & Yuan, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129163 · Cited by 88 · see citing works
Region‐ and Sex‐Specific Modulation of Anxiety Behaviours in the Rat
Toufexis, D. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2007.01552.x · Cited by 87 · see citing works
Steroid hormones, stress and the adolescent brain: A comparative perspective
Brown, G. R., & Spencer, K. A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.12.016 · Cited by 86 · see citing works
“21 Stress-induced CORT responses then decrease again in adulthood in rodents (Romeo, 2010b), 22 although not all results are consistent with this pattern across ages (e.g., Viau et al., 2005).”
Sex, stress and steroids
Sze, Y., & Brunton, P. J. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14615 · Cited by 85 · see citing works
“Puberty is accompanied by dynamic changes in circulating adrenal and gonadal steroids in males and females, which contribute to the organisation and maturation of the HPA axis (Viau et al., 2005).”
BackgroundResultInfluential
Divergent stress-induced neuroendocrine and behavioral responses prior to puberty
Lui, P., Padow, V. A., Franco, D., Hall, B. S., Park, B., Klein, Z. A., & Romeo, R. D. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.06.011 · Cited by 84 · see citing works
“The PVN was analyzed because previous reports indicated that the parv portion of the PVN displays differential neural activation in prepubertal and adult male rats following acute or homotypic stress paradigms [24,27].”
BackgroundMethod
Impact of maternal undernutrition on the hypothalamic–pituitary–adrenal axis responsiveness in sheep at different ages postnatal
Chadio, S. E., Kotsampasi, B., Papadomichelakis, G., Deligeorgis, S. G., Kalogiannis, D., Menegatos, I., & Zervas, G. (2007) · Journal of Endocrinology · doi:10.1677/joe-06-0172 · Cited by 82 · see citing works
Examination of peripheral basal and reactive cortisol levels in major depressive disorder and the burnout syndrome: A systematic review
Rothe, N., Steffen, J., Penz, M. S., Kirschbaum, C., & Walther, A. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.02.024 · Cited by 83 · see citing works
Sex Differences in the HPA Axis
Goel, N., Workman, J. L., Lee, T. T., Innala, L., & Viau, V. (2014) · Comprehensive physiology · doi:10.1002/j.2040-4603.2014.tb00575.x · Cited by 82 · see citing works
“in total corticosterone is paralleled by greater levels of ACTH in females following stress, as seen in numerous studies using psychological and physiological stressors (167, 199, 307, 309, 334, 381).”
InfluentialSelf-citation
An animal model of social instability stress in adolescence and risk for drugs of abuse
McCormick, C. M. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.01.014 · Cited by 76 · see citing works
A mechanistic hypothesis of the factors that enhance vulnerability to nicotine use in females
O’Dell, L. E., & Torres, O. V. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.055 · Cited by 74 · see citing works
Adolescent rats are protected from the conditioned aversive properties of cocaine and lithium chloride
Schramm‐Sapyta, N. L., Morris, R. W., & Kuhn, C. M. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.05.026 · Cited by 76 · see citing works
“…is thought to mediate anxiety in the EPM (Koob et al., 1993; Shepard et al., 2000), whereas CRF release in the hypothalamus stimulates the HPA axis cascade, leading to peripheral corticosterone release in a process affected by interindividual variation in testosterone levels (Viau et al., 2005).”
BackgroundInfluential
Sex and stress steroids in adolescence: Gonadal regulation of the hypothalamic–pituitary–adrenal axis in the rat
Green, M. R., & McCormick, C. M. (2016) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2016.02.004 · Cited by 76 · see citing works
Effects of a single footshock followed by situational reminders on HPA axis and behaviour in the aversive context in male and female rats
Louvart, H., Maccari, S., Lésage, J., Léonhardt, M., Dickès-Coopman, A., & Darnaudéry, M. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.05.014 · Cited by 72 · see citing works
Disruptive effects of repeated stress on basolateral amygdala neurons and fear behavior across the estrous cycle in rats
Blume, S. R., Padival, M., Urban, J. H., & Rosenkranz, J. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-48683-3 · Cited by 71 · see citing works
Differential Responses of the HPA Axis to Mild Blast Traumatic Brain Injury in Male and Female Mice
Russell, A. L., Mc, R., Bauman, B. M., Hernandez, I. M., Saperstein, S., Handa, R. J., & Wu, T. J. (2018) · Endocrinology · doi:10.1210/en.2018-00203 · Cited by 71 · see citing works
Early deprivation, but not maternal separation, attenuates rise in corticosterone levels after exposure to a novel environment in both juvenile and adult female rats
Rees, S. L., Steiner, M. S., & Fleming, A. S. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.09.013 · Cited by 71 · see citing works
Age of stress exposure modulates the immediate and sustained effects of repeated stress on corticolimbic cannabinoid CB1 receptor binding in male rats
Lee, T. T. Y., & Hill, M. N. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.017 · Cited by 67 · see citing works
“being said, there are several maturational changes that occur during puberty due to changes in gonadal hormones, such as changes in HPA axis function (Viau et al., 2005; Evuarherhe et al., 2009), that could in turn impact the regulation of CB1 receptor densities by stress during these different developmental periods.”
Background
Habituation of hypothalamic–pituitary–adrenocortical axis hormones to repeated homotypic stress and subsequent heterotypic stressor exposure in male and female rats
Babb, J. A., Masini, C. V., Day, H. E. W., & Campeau, S. (2014) · Stress · doi:10.3109/10253890.2014.905534 · Cited by 67 · see citing works
“stress-induced HPA axis hormone release following a variety of stressors compared to males (Aloisi et al., 1994, 1998; Babb et al., 2013a; Drossopoulou et al., 2004; Handa et al., 1994; Heinsbroek et al., 1991; Larkin et al., 2010; Le Mevel et al., 1978; Livezey et al., 1985; Ogilvie & Rivier, 1997; Seale et al., 2004…”
BackgroundInfluential
Translational relevance of rodent models of hypothalamic-pituitary-adrenal function and stressors in adolescence
McCormick, C. M., Green, M. R., & Simone, J. J. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.08.003 · Cited by 66 · see citing works
“…there are reports of greater corticosterone release in response to 30 min of restraint in prepubertal than in adult females (Romeo et al., 2004b; Viau et al., 2005), and a report of reduced corticosterone release at 15 and 30 min into a 90 min restraint session compared with adult females…”
The metamorphosis of adolescent hormonal stress reactivity: A focus on animal models
Romeo, R. D. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.12.003 · Cited by 63 · see citing works
“We and others find a greater number of FOS-positive cells in the PVN of stressed pre-adolescent animals compared to adults in response to either a single (Viau et al., 2005; Romeo et al., 2006a; Lui et al., 2012) or repeated exposure to restraint stress (Romeo et al.”
Background
Social subordination impairs hypothalamic–pituitary–adrenal function in female rhesus monkeys
Michopoulos, V., Reding, K. M., Wilson, M. E., & Toufexis, D. J. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.07.014 · Cited by 64 · see citing works
“…response, the simplest explanation is that in these studies, LHPA activity is modulated by hormonal status, as has been seen in rodents (Viau, 2002; Viau et al., 2001, 2005), monkeys (Stavisky et al., 2003; Wilson et al., 2005; Wood et al., 2004), and women (Burleson et al., 1998; Gudmundsson et…”
Background
A Comparison of Two Repeated Restraint Stress Paradigms on Hypothalamic‐Pituitary‐Adrenal Axis Habituation, Gonadal Status and Central Neuropeptide Expression in Adult Male Rats
Gray, M. E., Bingham, B., & Viau, V. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01941.x · Cited by 58 · see citing works
Self-citation
Organizational role for pubertal androgens on adult hypothalamic-pituitary-adrenal sensitivity to testosterone in the male rat
Evuarherhe, O., Leggett, J. D., Waite, E. J., Kershaw, Y. M., Atkinson, H. C., & Lightman, S. L. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.168393 · Cited by 61 · see citing works
Tolerance-inducing effect and properties of innate immune stimulation on chronic stress-induced behavioral abnormalities in mice
Gu, Y., Ye, T., Tan, P., Tong, L., Jian-lin, J., Gu, Y., Shen, Z., Shen, X., Lu, X., & Huang, C. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.11.002 · Cited by 59 · see citing works
Central organization of androgen-sensitive pathways to the hypothalamic-pituitary-adrenal axis: Implications for individual differences in responses to homeostatic threat and predisposition to disease
Williamson, M., Bingham, B., & Viau, V. (2005) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2005.08.009 · Cited by 58 · see citing works
Self-citation
Sex differences in serotonin (5-HT) 1A receptor regulation of HPA axis and dorsal raphe responses to acute restraint
Goel, N., Innala, L., & Viau, V. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.11.020 · Cited by 60 · see citing works
“Our results showed that females produce greater basal levels of ACTH and both basal and stress-induced levels of CORT compared to males, as previously observed (Goel and Bale, 2008; Handa et al., 1994; Viau et al., 2005).”
BackgroundResultSelf-citation
Androgen and estrogen receptor‐β distribution within spinal‐projecting and neurosecretory neurons in the paraventricular nucleus of the male rat
Bingham, B., Williamson, M., & Viau, V. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21151 · Cited by 58 · see citing works
“Estrogenic regulation of the HPA axis has also been consistently associated with alterations in medial parvocellular recruitment and anterior pituitary output (Dayas et al., 2000; Lund et al., 2004; Viau et al., 2005; but see Figueiredo et al., 2002).”
BackgroundSelf-citation
Stress, sex, and addiction
Bisagno, V., & Cadet, J. L. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000049 · Cited by 60 · see citing works
“Sex-dependent effects of corticotropinreleasing factor Preclinical studies have also shown that female rodents have higher basal levels of the glucocorticoid, corticosterone, than males (Weinstock et al., 1998; Viau et al., 2005).”
BackgroundInfluential
Cellular and molecular mechanisms of sexual differentiation in the mammalian nervous system
Forger, N. G., Strahan, J. A., & Castillo‐Ruiz, A. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.01.001 · Cited by 57 · see citing works
“The precise molecular mechanisms of gonadal hormone action on the HPA axis are yet to be identified, but female rats have a higher basal level of CRF mRNA in the PVN than do males (Duncko et al., 2001; Viau et al., 2005).”
Background
Glucocorticoid Receptor mRNA Expression in the Hippocampal Formation of Male Rats before and after Pubertal Development in Response to Acute or Repeated Stress
Romeo, R. D., Ali, F. S., Karatsoreos, I. N., Bellani, R., Chhua, N., Vernov, M., & McEwen, B. S. (2007) · Neuroendocrinology · doi:10.1159/000109710 · Cited by 56 · see citing works
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“Under non-BPA conditions, stress typically generates greater CORT release for a longer time period in female rather than male rodents (Handa et al., 1994a; Iwasaki-Sekino et al., 2009; Kitay, 1961; Viau et al., 2005).”
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Androgen receptor expressing neurons that project to the paraventricular nucleus of the hypothalamus in the male rat
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“…gene and its protein counterpart, Fos, within the PVN and several putative central regula- tors of the HPA axis (Da Costa et al., 1996; Kerr et al., 1996; Cheung et al., 1997; Nappi et al., 1997; Rachman et al., 1998; Figueiredo et al., 2002; Ceccarelli et al., 2003, 2006; Viau et al., 2003, 2005).”
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“…adrenal GC secretion is greater in females than in males (Kitay 1963, Critchlow et al, 1963, Handa et al, 1994a) and stimulation of the hypophysiotrophic stress response and PVN neuron activation are correspondingly higher in females (Larkin et al, 2010, Seale et al, 2004, Viau et al, 2005).”
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“Prior to puberty, when T levels are low, the CORT response to acute and chronic stress is high relative to the response seen after puberty (Viau et al., 2005; Romeo and McEwen, 2006; Follib et al., 2011).”
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“Along similar lines, female rodents display larger increases in corticosterone secretion (Goel et al., 2014; Viau et al., 2005), and use different behavioral strategies than males in response to a variety of challenges (Goel et al.”
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Stressor-specific effects of sex on HPA axis hormones and activation of stress-related neurocircuitry
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“…including foot- or tail-shock (Bland et al., 2005; Heinsbroek et al., 1991; Rivier, 1991), neonatal handling (Panagiotaropoulous et al., 2004), restraint (Aloisi et al., 1994; 1998; Babb et al., 2013; Le Mevel et al., 1979; Viau et al., 2005), and immune challenge (Seale et al., 2004a, b).”
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Corticotrophin‐Releasing Factor Alters the Timing of Puberty in the Female Rat
Kinsey‐Jones, J. S., Li, X. F., Knox, A. M. I., Lin, Y., Milligan, S. R., Lightman, S. L., & O’Byrne, K. T. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01940.x · Cited by 51 · see citing works
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CRHR1 Polymorphisms Predict Bone Density in Survivors of Acute Lymphoblastic Leukemia
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Pubertal- and Stress-Dependent Changes in Cellular Activation and Expression of Excitatory Amino Acid Receptor Subunits in the Paraventricular Nucleus of the Hypothalamus in Male and Female Rats
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Stress-Induced Activation of Orexin-A Neurons in the Lateral Hypothalamus Is Similar in Prepubertal and Adult Male and Female Rats despite Age-Dependent Differences in Hormonal Stress Reactivity
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Differential Stress Reactivity in Intact and Ovariectomized Prepubertal and Adult Female Rats
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Stress History and Pubertal Development Interact to Shape Hypothalamic-Pituitary-Adrenal Axis Plasticity
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Authors: Viau, V., Bingham, B., Davis, J., Lee, P., & Wong, M.
Affiliations: University of British Columbia (CA)
Corresponding author: Viau, Victor
ORCID: Viau, Victor
Davis, Jennifer
Lee, Patricia
Venue: Endocrinology
Publisher: The Endocrine Society
Published: 2005-01-01
Volume: 146
Issue: 1
Pages: 137-146
ISSN: 0013-7227 (ISSN-L)
1945-7170
DOI: 10.1210/en.2004-0846
OpenAlex: W2159178030
Cited by: 266
References: 59
Citations by year: 2026: 10 · 2025: 7 · 2024: 8 · 2023: 12 · 2022: 14 · 2021: 22 · 2020: 13 · 2019: 15 · 2018: 10 · 2017: 11 · 2016: 17 · 2015: 13 · 2014: 13 · 2013: 16 · 2012: 14
FWCI: 3.66
Type: journal article
Language: en
Open access: closed
Locations: Endocrinology (publishedVersion)
PubMed (publishedVersion)
Funders: Michael Smith Health Research BC
Canadian Institutes of Health Research
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords: puberty, sex differences, hypothalamic-pituitary-adrenal axis, corticotropin-releasing factor, paraventricular nucleus, parvocellular neurons, vasopressin, Fos protein, restraint stress, central amygdala, age-related changes, neurosecretion, rats
MeSH terms: Amygdala, Animals, Arginine Vasopressin, Corticotropin-Releasing Hormone, Female, Gonads, Male, Paraventricular Hypothalamic Nucleus, Pituitary-Adrenal System, Restraint, Physical, RNA, Heterogeneous Nuclear, RNA, Messenger, Sex Characteristics, Stress, Physiological, Proto-Oncogene Proteins c-fos, Rats, Sprague-Dawley, Rats

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Gender and puberty interact on the stress-induced activation of parvocellular neurosecretory neurons and corticotropin-releasing hormone messenger ribonucleic acid expression in the rat

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