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The Pulsatile Characteristics of Hypothalamo-Pituitary-Adrenal Activity in Female Lewis and Fischer 344 Rats and Its Relationship to Differential Stress Responses*
Abstract
The dynamic patterns of basal and stimulated hypothalamo-pituitary-adrenal (HPA) activity of freely moving female Lewis and Fischer 344 rats were compared using an automated blood-sampling system. Both strains showed pulsatile corticosterone release throughout the 24 h cycle. Lewis rats showed clear circadian variation in both pulse frequency (8.4 +/- 0.4 pulses between 1700-2300 h vs. 5.3 +/- 0.8 pulses between 0500-1100 h; P < 0.05) and height (198 +/- 27 ng/ml between 1700-2300 h vs. 107 +/- 14 ng/ml between 0500-1100 h; P < 0.05). Fischer rats exhibited pulses of similar frequency and height to those in Lewis rats during the evening, but showed no circadian variation, resulting in higher mean daily corticosterone concentrations. Although both strains showed behavioral and HPA responses to white noise stress (10 min; 114 dB), Fischer rats showed much greater increases in total activity, grooming, and rearings, and two important differences in the corticosterone responses were observed. First, in Lewis rats a clear relationship existed between basal and stimulated HPA activities, in that a significant response was seen only when the stress coincided with the rising (secretory active) phase of a basal pulse. Noise stress coinciding with a falling (nonsecretory) phase elicited no significant response. In contrast, Fischer rats showed similar responses regardless of the underlying pulse phase. Second, after the peak response at 20 min (Lewis, 237 +/- 67 ng/ml; Fischer, 390 +/- 57 ng/ml), corticosterone levels fell rapidly in Lewis rats, but remained maximally elevated for 20 min in Fischer rats, resulting in a significantly greater integrated response. The corticosterone response to i.v. CRF was unaffected by pulse phase in both strains, suggesting that a suprapituitary mechanism mediates the phase-dependent response to stress in the Lewis strain. CRF-induced corticosterone levels rose more rapidly in Fischer rats, peaking at 10 min (473 +/- 95 ng/ml) compared with 30 min (390 +/- 75 ng/ml) in Lewis rats, suggesting greater pituitary sensitivity in this strain. Thus, differences in both central and pituitary control of the HPA axis contribute to the strain difference in stress responsiveness between female Lewis and Fischer rats.
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“the timing of an incoming stressor, relative to the phase of an endogenous pulse of CORT, has been shown to govern the amplitude of the subsequent stress response as well as the timing of subsequent pulses [1,12].”
From Rapid intra-adrenal feedback regulation of glucocorticoid synthesis (2015) · cites this paper as [1]
In the citing paper
“new experimental [9-15] and theoretical [16-27] results offer enough evidence to support the indispensable roles of ultradian oscillatory dynamics of HPA hormones levels for normal physiology.”
From Predictive modeling of the hypothalamic-pituitary-adrenal (HPA) axis response to acute and chronic stress (2011) · cites this paper as [14]
In the citing paper
“the same acute stress (5 min white noise stress of 114 dB) applied either in the ascending (secreting) and interpulse phase or during the descending (non-secreting) phase of corticosterone ultradian rhythm evoked significant increase of corticosterone level only when it had been applied during the ascending [13-15] or interpulse [15] phase of ultradian basal corticosterone pulse.”
From Predictive modeling of the hypothalamic-pituitary-adrenal (HPA) axis response to acute and chronic stress (2011) · cites this paper as [14]
In the citing paper
“there are several experimental observa -tions showing that acute stress induces different effects depending on the phase of the ultradian secretion pulse at which the stress has been induced [11, 13-15].”
From Predictive modeling of the hypothalamic-pituitary-adrenal (HPA) axis response to acute and chronic stress (2011) · cites this paper as [14]
In the citing paper
“according to which the HPA axis response to stress depends on the ultradian phase (Fig. 2)”
From Predictive modeling of the hypothalamic-pituitary-adrenal (HPA) axis response to acute and chronic stress (2011) · cites this paper as [14]
In the citing paper
“intravenous injection of specific dosage of CRH (2 μg) administered to rats during the rising or falling phase of the corticosterone ultradian oscillations failed to induce significant difference between the two rat groups [14].”
From Predictive modeling of the hypothalamic-pituitary-adrenal (HPA) axis response to acute and chronic stress (2011) · cites this paper as [14]
In the citing paper
“Numerical simulations (Figs. 2, 3) reproduced the empirically well established notion that the same stimulus applied at slightly different time points, may induce different, even opposite changes in cortisol levels in the same individual [13-15].”
From Predictive modeling of the hypothalamic-pituitary-adrenal (HPA) axis response to acute and chronic stress (2011) · cites this paper as [14]
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“obtained from visual inspection of the data, as recommended (Windle et al., 1998).”
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Conway-Campbell, B. L., George, C. L., Pooley, J. R., Knight, D. M., Norman, M. R., Hager, G. L., & Lightman, S. L. (2011) · Molecular Endocrinology · doi:10.1210/me.2010-0073 · Cited by 67
Self-citationMolecular genetics of hypothalamic–pituitary–adrenal axis activity and function
Mormède, P., Foury, A., Barat, P., Corcuff, J., Terenina, E. E., Marissal‐Arvy, N., & Moisan, M. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05902.x · Cited by 68
Thanos, P. K., Cavigelli, S., Michaelides, M., Olvet, D. M., Patel, U., Diep, M., & Volkow, N. D. (2009) · Physiological Research · doi:10.33549/physiolres.931434 · Cited by 67
Rhythmicity matters: Circadian and ultradian patterns of HPA axis activity
Focke, C. M. B., & Iremonger, K. J. (2019) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2019.110652 · Cited by 64
Droste, S. K., De Groote, L., Lightman, S. L., Reul, J. M. H. M., & Linthorst, A. C. E. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01811.x · Cited by 61
Self-citationMobbing vocalizations as a coping response in the common marmoset
Cross, N., & Rogers, L. J. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.07.007 · Cited by 61
Dynamics of adrenal glucocorticoid steroidogenesis in health and disease
Spiga, F., & Lightman, S. L. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.02.005 · Cited by 63
“Further, analysis of corticosterone pulse characteristics using the PULSAR algorithm (Merriam and Wachter, 1982) has shown that the pulse amplitude varies in a circadian manner, with low amplitudes in the morning and higher amplitudes in the evening (Windle et al., 1998a).”
InfluentialSelf-citationRankin, J., Walker, J. J., Windle, R., Lightman, S. L., & Terry, J. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030978 · Cited by 60
“In the late 1990s, investigations into the effect of acute stress on the amplitude of the CORT response were performed using three strains of rat: female Sprague-Dawley (SD) [10], female Lewis [11], and male Piebald-Viral-Glaxo (PVG) with induced arthritis [12].”
MethodInfluentialSelf-citationEvuarherhe, 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
“Previous findings have reported maximal corticosterone secretion occurring 20 min post noise-stress onset (Windle et al. 1998).”
BackgroundSelf-citationMarkovic, V. M., Cupic, Z., Vukojevic, V., & Kolar-Anic, L. (2011) · Endocrine Journal · doi:10.1507/endocrj.ej11-0037 · Cited by 54
“2), there are several experimental observations showing that acute stress induces different effects depending on the phase of the ultradian secretion pulse at which the stress has been induced [11, 13-15].”
BackgroundMethodResultInfluentialLowry, C. A., Plant, A., Shanks, N. M., Ingram, C. D., & Lightman, S. L. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(02)00009-0 · Cited by 54
Self-citationDynamic access of the glucocorticoid receptor to response elements in chromatin
George, A. A., Schiltz, R. L., & Hager, G. L. (2008) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2008.09.019 · Cited by 54
Spiga, F., Harrison, L. R., Wood, S. A., Atkinson, H. C., MacSweeney, C. P., Thomson, F., Craighead, M., Grassie, M., & Lightman, S. L. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2007.01605.x · Cited by 53
Self-citationEmerging role of amyloid beta in stress response: Implication for depression and diabetes
Morgese, M. G., Schiavone, S., & Trabace, L. (2017) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2017.08.031 · Cited by 54
Sixty Years after Hench—Corticosteroids and Chronic Inflammatory Disease
Edwards, C. R. W. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-2879 · Cited by 52
“This has been confirmed by studies on the circadian rhythm of corticosterone in these two strains (49), with normal circadian rhythm in the Lewis rat that is absent in the Fischer rat.”
BackgroundCRH in chronic inflammatory stress
Jessop, D. S., Harbuz, M. S., & Lightman, S. L. (2001) · Peptides · doi:10.1016/s0196-9781(01)00394-1 · Cited by 49
Self-citationGlucocorticoid pulsatility and rapid corticosteroid actions in the central stress response
Sarabdjitsingh, R. A., Joëls, M., & de Kloet, E. R. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.09.017 · Cited by 50
“Also, clear genetic influences on the rhythm are found in strains of rats that differ in stress responsiveness and in their susceptibility to autoimmune disease [41].”
BackgroundUltradian Cortisol Pulsatility Encodes a Distinct, Biologically Important Signal
McMaster, A., Jangani, M., Sommer, P., Han, N., Brass, A., Beesley, S., Lu, W., Berry, A. A., Loudon, A. S. I., Donn, R. P., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0015766 · Cited by 49
“The existence of pulsatile release of glucocorticoids from the adrenal glands, and the attendant pulsatility of serum levels have been known for some time [13].”
BackgroundMethodBroin, F. D., Côté, S. D., Whiteside, D. P., & Mastromonaco, G. F. (2019) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2019.04.022 · Cited by 49
“Glucocorticoid concentrations have traditionally been measured in blood serum or plasma, but pulsatile fluctuations (Windle et al., 1998) and capture/restraint increase of GC concentration in the blood (Müller”
BackgroundSex, stress, and prefrontal cortex: influence of biological sex on stress-promoted cocaine seeking
Doncheck, E. M., Liddiard, G. T., Konrath, C. D., Liu, X., Yu, L., Urbanik, L. A., Herbst, M. R., DeBaker, M. C., Raddatz, N. J., Newenhizen, E. C. V., et al. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0674-3 · Cited by 45
Li, X. F., Edward, J., Mitchell, J. C., Shao, B., Bowes, J., Coen, C. W., Lightman, S. L., & O'Byrne, K. T. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2004.01209.x · Cited by 45
Self-citationVarejão, A. S. P., Cabrita, A., Geuna, S., Patrício, J., Azevedo, H. R., Ferreira, A., & Meek, M. F. (2003) · Microsurgery · doi:10.1002/micr.10148 · Cited by 44
Kearns, D. N., Gomez-Serrano, M. A., Weiss, S. J., & Riley, A. L. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.01.005 · Cited by 43
Fischer 344 and Lewis Rat Strains as a Model of Genetic Vulnerability to Drug Addiction
Cadoni, C. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00013 · Cited by 42
“…depending on sex, with female LEW rats showing circadian variation of CORT plasma concentrations which was not present in female F344 rats (Griffin andWhitacre, 1991; Windle et al., 1998), thus affecting CORT response to stress stimuli depending on the phase (rising or falling) of the basal pulse.”
BackgroundSpiga, F., Harrison, L. R., Wood, S., Knight, D. M., MacSweeney, C. P., Thomson, F., Craighead, M., & Lightman, S. L. (2009) · Journal of Endocrinology · doi:10.1677/joe-08-0421 · Cited by 40
Self-citationOnset and severity of inflammation in rats exposed to the learned helplessness paradigm
Chover-González, A. J., Jessop, D. S., Tejedor‐Real, P., Gibert‐Rahola, J., & Harbuz, M. S. (2000) · Lara D. Veeken · doi:10.1093/rheumatology/39.7.764 · Cited by 40
Scheff, J. D., Calvano, S. E., Lowry, S. F., & Androulakis, I. P. (2011) · Physiological Genomics · doi:10.1152/physiolgenomics.00128.2011 · Cited by 40
“As has been seen experimentally (53, 54), there is a strong dependence on the response to a stressor depending on whether the stressor occurs in the rising of falling GC phase.”
BackgroundResultMichaud, D. S., McLean, J., Keith, S. E., Ferrarotto, C., Hayley, S. P., Khan, S. A., Anisman, H., & Merali, Z. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300149 · Cited by 39
“The observed behavioral response to noise exposure in the present study was very similar to that reported by Windle et al (1998) where female Fischer and Lewis rats displayed striking differences in their behavioral response to loud noise.”
BackgroundResultInfluentialIndividual variation in cortisol responses to acute ‘on-back’ restraint in an outbred hamster
Guimont, F., & Wynne‐Edwards, K. E. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.03.008 · Cited by 35
Sarabdjitsingh, R. A., Spiga, F., Oitzl, M. S., Kershaw, Y., Meijer, O. C., Lightman, S. L., & De Kloet, E. R. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.02004.x · Cited by 35
Self-citationStress and the Reproductive System
Ferin, M. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50053-1 · Cited by 35
Mason, D. R., Hassan, A. H., Chacko, S. K., & Thompson, P. (2002) · Archives of Physiology and Biochemistry · doi:10.1076/apab.110.1.74.905 · Cited by 34
“VP, CRH, ACTH, and glucocorticoids have all been shown to be secreted in an ultradian pulsatile fashion (Engler et al., 1989b; Alexander et al., 1994; Ixart et al., 1991; Windle et al., 1998), with peripheral plasma concentrations of glucocorticoids and ACTH exhibiting circadian as well as ultradian rhythms (Carnes et…”
BackgroundInfluence of indoor-cat group size and dominance rank on urinary cortisol levels
Lichtsteiner, M., & Turner, D. C. (2008) · Animal Welfare · doi:10.1017/s0962728600032152 · Cited by 34
“For example, high human density might lead to a high noise level in the household which in turn might elevate basal cortisol levels of the cats, as was shown in rats (Windle et al 1998), dogs (Beerda et al 1998), and humans (Melamed & Bruhis 1996).”
Corticosterone modulation of somatodendritic 5-HT1A receptor function in mice
Man, M., Young, A. H., & McAllister-Williams, H. (2002) · Journal of Psychopharmacology · doi:10.1177/026988110201600310 · Cited by 34
Metadata
- Authors
- Windle, R. J., Wood, S. A., Lightman, S. L., & Ingram, C. D.
- Affiliations
- Bristol Royal Infirmary (GB)
- University of Bristol (GB)
- Corresponding author
- Windle, R. J.
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 1998-10-01
- Volume
- 139
- Issue
- 10
- Pages
- 4044-4052
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- OpenAlex
- W1987343103
- Cited by
- 201
- References
- 52
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 2 · 2022: 2 · 2021: 4 · 2020: 9 · 2019: 9 · 2018: 2 · 2017: 4 · 2016: 10 · 2015: 6 · 2014: 8 · 2013: 6 · 2012: 8
- FWCI
- 2.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- hypothalamic-pituitary-adrenal axis, circadian variation, corticotropin-releasing factor, strain differences, Lewis rats, F344 rats, female rats, behavioral stress response, automated blood sampling
- MeSH terms
- Animals, Circadian Rhythm, Corticosterone, Corticotropin-Releasing Hormone, Female, Hypothalamo-Hypophyseal System, Pituitary-Adrenal System, Rats, Inbred F344, Rats, Inbred Lew, Species Specificity, Stress, Physiological, Rats
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