Strain specific behavioral and physiological responses to constant light in male CBA/J and CBA/CaJ mice

 

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Objective: Being visually impaired increases the likelihood of sleep disorders and altered behavior. This study investigated physiological and behavioral differences in two similar mice substrains when exposed to constant light (LL) - CBA/J with retinal degeneration and CBA/CaJ mice (no retinal degeneration).

Material and Methods: Male CBA/J and CBA/CaJ mice were placed into a 12:12 light:dark cycle or constant light (LL). Open field behavior, metabolic markers, and home-cage circadian activity were observed.

Results: CBA/CaJ mice have greater circadian period lengthening, increased weight gain, reduced glucose, and increased novelty-induced locomotor activity in LL, compared to CBA/J mice. LL reduced thyroid hormone and insulin in both substrains.

Discussion: While several baseline substrain differences were elucidated, CBA/CaJ mice were more effected by the exposure to LL than the blind CBA/J mice. These results illustrate that LL causes alterations in physiology and behavior and that circadian photoreceptivity might contribute to these effects.

Publication History

Received: 18 August 2020

Accepted: 28 December 2020

Article published online:
30 November 2023

© 2023. Brazilian Sleep Association. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

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• REFERENCES

• 1 Tapia-Osorio A, Salgado-Delgado R, Angeles-Castellanos M, Escobar C. Disruption of circadian rhythms due to chronic constant light leads to depressive and anxiety-like behaviors in the rat. Behav Brain Res. 2013 Sep;252:1-9.
• 2 Capri KM, Maroni MJ, Deane HV, Concepcion HA, DeCourcey H, Logan RW, et al. Male C57BL6/N and C57BL6/J mice respond differently to constant light and running-wheel access. Front Behav Neurosci. 2019;13:268.
• 3 Maroni MJ, Capri KM, Cushman AV, Pina IKM, Chasse MH, Seggio JA. Constant light alters serum hormone levels related to thyroid function in male CD-1 mice. Chronobiol Int. 2018 Jun;35(10):1456-63.
• 4 Gil-Lozano M, Hunter PM, Behan LA, Gladanac B, Casper RF, Brubaker PL. Short-term sleep deprivation with nocturnal light exposure alters time-dependent glucagon-like peptide-1 and insulin secretion in male volunteers. Am J Physiol Endocrinol Metab. 2016 Jan;310(1):E41-50.
• 5 Fernandez DC, Fogerson PM, Ospri LL, Thomsen MB, Layne RM, Severin D, et al. Light affects mood and learning through distinct retinabrain pathways. Cell. 2018 Sep;175(1):71-84.e18.
• 6 McHill AW, Melanson EL, Higgins J, Connick E, Moehlman TM, Stothard ER, et al. Impact of circadian misalignment on energy metabolism during simulated nightshift work. Proc Natl Acad Sci U S A. 2014 Dec;111(48):17302-7.
• 7 Flynn-Evans EE, Tabandeh H, Skene DJ, Lockley SW. Circadian rhythm disorders and melatonin production in 127 blind women with and without light perception. J Biol Rhythms. 2014 Jun;29(3):215-24.
• 8 Wee R, Castrucci AM, Provencio I, Gan L, Van Gelder RN. Loss of photic entrainment and altered free-running circadian rhythms in math5-/-mice. J Neurosci. 2002 Dec;22(23):10427-33.
• 9 Panda S, Provencio I, Tu DC, Pires SS, Rollag MD, Castrucci AM, et al. Melanopsin is required for non-image-forming photic responses in blind mice. Science. 2003 Jul;301(5632):525-7.
• 10 Yoshimura T, Ebihara S. Spectral sensitivity of photoreceptors mediating phase-shifts of circadian rhythms in retinally degenerate CBA/J (rd/rd) and normal CBA/N (+/+)mice. J Comp Physiol A. 1996 May;178(6):797-802.
• 11 Yoshimura T, Ebihara S. Decline of circadian photosensitivity associated with retinal degeneration in CBA/J-rd/rd mice. Brain Res. 1998 Jan;779(1-2):188-93.
• 12 Yoshimura T, Nishio M, Goto M, Ebihara S. Differences in circadian photosensitivity between retinally degenerate CBA/J mice (rd/rd) and normal CBA/N mice (+/+). J Biol Rhythms. 1994 Mar;9(1):51-60.
• 13 Nascimento NF, Hicks JA, Carlson KN, Hatzidis A, Amaral DN, Logan RW, et al. Long-term wheel-running and acute 6-h advances alter glucose tolerance and insulin levels in TALLYHO/JngJ mice. Chronobiol Int. 2016;33(1):108-16.
• 14 Hicks JA, Hatzidis A, Arruda NL, Gelineau RR, Pina IM, Adams KW, et al. Voluntary wheel-running attenuates insulin and weight gain and affects anxiety-like behaviors in C57BL6/J mice exposed to a high-fat diet. Behav Brain Res. 2016 Sep;310:1-10.
• 15 Ruby NF, Brennan TJ, Xie X, Cao V, Franken P, Heller HC, et al. Role of melanopsin in circadian responses to light. Science. 2002 Dec;298(5601):2211-3.
• 16 Lockley SW, Arendt J, Skene DJ. Visual impairment and circadian rhythm disorders. Dialogues Clin Neurosci. 2007;9(3):301-14.
• 17 Steinlechner S, Jacobmeier B, Scherbarth F, Dernbach H, Kruse F, Albrecht U. Robust circadian rhythmicity of Per1 and Per2 mutant mice in constant light, and dynamics of Per1 and Per2 gene expression under long and short photoperiods. J Biol Rhythms. 2002 Jun;17(3):202-9.
• 18 Ruggiero L, Allen CN, Brown RL, Robinson DW. Mice with early retinal degeneration show differences in neuropeptide expression in the suprachiasmatic nucleus. Behav Brain Funct. 2010;6:36.
• 19 Ruggiero L, Allen CN, Brown RL, Robinson DW. The development of melanopsin-containing retinal ganglion cells in mice with early retinal degeneration. Eur J Neurosci. 2009 Jan;29(2):359-67.
• 20 Albers HE, Minamitani N, Stopa E, Ferris CF. Light selectively alters vasoactive intestinal peptide and peptide histidine isoleucine immunoreactivity within the rat suprachiasmatic nucleus. Brain Res. 1987 Dec;437(1):189-92.
• 21 Isobe Y, Nishino H. AVP rhythm in the suprachiasmatic nucleus in relation to locomotor activity under constant light. Peptides. 1998;19(5):827-32.
• 22 Foster RG, Provencio I, Hudson D, Fiske S, Grip W, Menaker M. Circadian photoreception in the retinally degenerate mouse (rd/rd). J Comp Physiol A. 1991 Jul;169(1):39-50.
• 23 Agostino PV, Nascimento M, Bussi IL, Eguia MC, Golombek DA. Circadian modulation of interval timing in mice. Brain Res. 2011 Jan;1370:154-63.
• 24 Acosta J, Bussi IL, Esquivel M, Hocht C, Golombek DA, Agostino PV. Circadian modulation of motivation in mice. Behav Brain Res. 2020 Mar;382:112471.
• 25 McGowan NM, Coogan AN. Circadian and behavioural responses to shift work-like schedules of light/dark in the mouse. J Mol Psychiatry. 2013 May;1(1):7.
• 26 Ohta H, Yamazaki S, McMahon DG. Constant light desynchronizes mammalian clock neurons. Nat Neurosci. 2005 Mar;8(3):267-9.
• 27 Karatsoreos IN, Bhagat S, Bloss EB, Morrison JH, McEwen BS. Disruption of circadian clocks has ramifications for metabolism, brain, and behavior. Proc Natl Acad Sci U S A. 2011 Jan;108(4):1657-62.
• 28 Maroni MJ, Capri KM, Arruda NL, Gelineau RR, Deane HV, Concepcion HA, et al. Substrain specific behavioral responses in male C57BL/6N and C57BL/6J mice to a shortened 21-hour day and highfat diet. Chronobiol Int. 2020 May;37(6):809-23.
• 29 Celec P, Ostatnikova D, Hodosy J. On the effects of testosterone on brain behavioral functions. Front Neurosci. 2015;9:12.
• 30 Adler A, Vescovo P, Robinson JK, Kritzer MF. Gonadectomy in adult life increases tyrosine hydroxylase immunoreactivity in the prefrontal cortex and decreases open field activity in male rats. Neuroscience. 1999 Mar;89(3):939-54.
• 31 Raynaud J, Schradin C. Experimental increase of testosterone increases boldness and decreases anxiety in male African striped mouse helpers. Physiol Behav. 2014 Apr;129:57-63.
• 32 Faraut B, Andrillon T, Drogou C, Gauriau C, Dubois A, Servonnet A, et al. Daytime exposure to blue-enriched light counters the effects of sleep restriction on cortisol, testosterone, alpha-amylase and executive processes. Front Neurosci. 2019;13:1366.
• 33 Vinogradova IA, Anisimov VN, Bukalev AV, Semenchenko AV, Zabezhinski MA. Circadian disruption induced by light-at-night accelerates aging and promotes tumorigenesis in rats. Aging (Albany NY). 2009 Oct;1(10):855-65.
• 34 Connelly DM, Taberner PV. Characterization of the spontaneous diabetes obesity syndrome in mature male CBA/Ca mice. Pharmacol Biochem Behav. 1989 Oct;34(2):255-9.
• 35 Boden G, Chen X, Polansky M. Disruption of circadian insulin secretion is associated with reduced glucose uptake in first-degree relatives of patients with type 2 diabetes. Diabetes. 1999 Nov;48(11):2182-8.
• 36 Mantele S, Otway DT, Middleton B, Bretschneider S, Wright J, Robertson MD, et al. Daily rhythms of plasma melatonin, but not plasma leptin or leptin mRNA, vary between lean, obese and type 2 diabetic men. PLoS One. 2012;7(5):e37123.
• 37 Nicoletti F, Di Marco R, Barcellini W, Borghi MO, Lunetta M, Mughini L, et al. Protection from experimental autoimmune thyroiditis in CBA mice with the novel immunosuppressant deoxyspergualin. Scand J Immunol. 1994 Mar;39(3):333-6.
• 38 Coomans CP, Van Den Berg SA, Houben T, Van Klinken JB, Van Den Berg R, Pronk AC, et al. Detrimental effects of constant light exposure and high-fat diet on circadian energy metabolism and insulin sensitivity. FASEB J. 2013 Apr;27(4):1721-32.
• 39 Maroni MJ, Capri KM, Cushman AV, Deane HV, Concepcion H, DeCourcey H, et al. The timing of fasting leads to different levels of food consumption and PYY. Hormones (Athens). 2020 Jun;19:549-58.
• 40 Qian J, Yeh B, Rakshit K, Colwell CS, Matveyenko AV. Circadian disruption and diet-induced obesity synergize to promote development of β-cell failure and diabetes in male rats. Endocrinology. 2015 Dec;156(12):4426-36.