Original Article

Impact of Exposure to Environmental Enrichment on the Anxiety-Like Behavior of Ovariectomized Mice

Abstract

Objective: The aim of this study was to explore the influence of short-term (2-week) exposure to social (SE) and/or physical enrichment (PE) on the anxiety-like behavior of ovariectomized (OVX) NIH Swiss mice.
Method: One week after surgery, each OVX mouse was housed under one of 4 social conditions: (1) isolated, (2) accompanied by an intact female, (3) accompanied by an intact male, or (4) in a community of 10 OVX individuals. The animals in each of these environments were divided into 2 subgroups, consisting of the presence and absence of PE. Following a 2-week exposure to the respective conditions, each OVX mouse was subjected to either the light/dark exploration test (LDT) or the elevated plus maze (EPM) to examine anxiety-like behavior.
Results: The LDT and EPM showed very similar patterns. Compared to an impoverished environment, PE elicited a significant anxiolytic effect for OVX mice housed alone or in companion of an intact female (F [1, 54] = 16.11, P = 0.001). By contrast, mice living in community but without PE displayed anxiogenic-like behavior, perhaps due to crowding, compared to the animals living in isolation (F [1, 36] = 5.64, P = 0.023).
Conclusion: This study emphasized the importance of taking housing conditions into account during the screening of new anxiolytic agents and the critical role of OVX in the regulation of anxiety.

Anchan D, Clark S, Pollard K, Vasudevan N. GPR30 activation decreases anxiety in the open field test but not in the elevated plus maze test in female mice. Brain Behav 2014;4: 51-9.

Morgan MA, Pfaff DW. Effects of estrogen on activity and fear-related behaviors in mice. Horm Behav 2001;40: 472-82.

Patki G, Allam FH, Atrooz F, Dao AT, Solanki N, Chugh G, et al.Grape powder intake prevents ovariectomy-induced anxiety-like behavior, memory impairment and high blood pressure in female Wistar rats. PLoS One 2013;8: e74522.

Frye CA, Walf AA. Estrogen and/or progesterone administered systemically or to the amygdala can have anxiety-, fear-, and pain-reducing effects in ovariectomized rats. Behav Neurosci 2004;118: 306-13.

Llaneza DC, Frye CA. Progestogens and estrogen influence impulsive burying and avoidant freezing behavior of naturally cycling and ovariectomized rats. Pharmacol Biochem Behav 2009;93: 337-42.

Daendee S, Thongsong B, Kalandakanond-Thongsong S. Effects of time of estrogen deprivation on anxiety-like behavior and GABAA receptor plasticity in ovariectomized rats. Behav Brain Res 2013;246: 86-93.

Picazo O, Estrada-Camarena E, Hernandez-Aragon A. Influence of the post-ovariectomy time frame on the experimental anxiety and the behavioural actions of some anxiolytic agents. Eur J Pharmacol 2006;530: 88-94.

Mora S, Dussaubat N, Díaz-Véliz G. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 1996;21: 609-20.

Galeeva A, Tuohimaa P. Analysis of mouse plus-maze behavior modulated by ovarian steroids. Behav Brain Res 2001;119: 41-7.

Jones AB, Gupton R, Curtis KS. Estrogen and voluntary exercise interact to attenuate stress-induced corticosterone release but not anxiety-like behaviors in female rats. Behav Brain Res 2016;311: 279-286.

Zimmermann A, Stauffacher M, Langhans W, Würbel H. Enrichment-dependent differences in novelty exploration in rats can be explained by habituation. Behav Brain Res 2001;121: 11-20.

Nakayasu T, Ishii K. Effects of pair-housing after social defeat experience on elevated plus-maze behavior in rats. Behav Processes 2008;78: 477-80.

Peña Y, Prunell M, Dimitsantos V, Nadal R, Escorihuela RM. Environmental enrichment effects in social investigation in rats are gender dependent. Behav Brain Res 2006;174: 181-7.

Cao M, Pu T, Wang L, Marshall C, He H, Hu G, et al. Early enriched physical environment reverses impairments of the hippocampus, but not medial prefrontal cortex, of socially-isolated mice. Brain Behav Immun 2017;64: 232-243.

Pritchard LM, Van Kempen TA, Zimmerberg B. Behavioral effects of repeated handling differ in rats reared in social isolation and environmental enrichment. Neurosci Lett 2013;536: 47-51.

Hughes RN, Otto MT. Anxiolytic effects of environmental enrichment attenuate sex-related anxiogenic effects of scopolamine in rats. Prog Neuropsychopharmacol Biol Psychiatry 2013;40: 252-9.

Meng FT, Zhao J, Ni RJ, Fang H, Zhang LF, Zhang Z, et al. Beneficial effects of enriched environment on behaviors were correlated with decreased estrogen and increased BDNF in the hippocampus of male mice. Neuro Endocrinol Lett. 2015;36: 490-7.

Islas-Preciado D, López-Rubalcava C, González-Olvera J, Gallardo-Tenorio A, Estrada-Camarena E. Environmental enrichment prevents anxiety-like behavior induced by progesterone withdrawal in two strains of rats. Neuroscience 2016;336: 123-132.

Zubedat S, Aga-Mizrachi S, Cymerblit-Sabba A, Ritter A, Nachmani M, Avital A. Methylphenidate and environmental enrichment ameliorate the deleterious effects of prenatal stress on attention functioning. Stress 2015;18: 280-8.

Abramov U, Puussaar T, Raud S, Kurrikoff K, Vasar E. Behavioural differences between C57BL/6 and 129S6/SvEv strains are reinforced by environmental enrichment. Neurosci Lett 2008;443: 223-7.

van de Weerd HA, Baumans V, Koolhaas JM, van Zutphen LF. Strain specific behavioural response to environmental enrichment in the mouse. J Exp Anim Sci 1994;36: 117-27.

Elliott BM, Grunberg NE. Effects of social and physical enrichment on open field activity differ in male and female Sprague-Dawley rats. Behav Brain Res 2005;165: 187-96.

Hendershott TR, Cronin ME, Langella S, McGuinness PS, Basu AC. Effects of environmental enrichment on anxiety-like behavior, sociability, sensory gating, and spatial learning in male and female C57BL/6J mice. Behav Brain Res 2016;314: 215-25.

Gresack JE, Kerr KM, Frick KM. Short-term environmental enrichment decreases the mnemonic response to estrogen in young, but not aged, female mice. Brain Res 2007;1160: 91-101.

Rehbinder C, Baneux P, Forbes D, van Herck H, Nicklas W, Rugaya Z, et al. FELASA recommendations for the health monitoring of mouse, rat, hamster, gerbil, guinea pig and rabbit experimental units. Report of the Federation of European Laboratory Animal Science Associations (FELASA) Working Group on Animal Health accepted by the FELASA Board of Management, November 1995. Lab Anim 1996;30: 193-208.

Briones-Aranda A, López-Rubalcava C, Picazo O. Influence of forced swimming-induced stress on the anxiolytic-like effect of 5HT(1A) agents in mice. Psychopharmacology (Berl) 2002;162: 147-55.

Briones-Aranda A, Rocha L, Picazo O. Alterations in GABAergic function following forced swimming stress. Pharmacol Biochem Behav 2005;80: 463-70.

Crawley J, Goodwin FK. Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 1980;13: 167-70.

Budzynska B, Boguszewska-Czubara A, Kruk-Slomka M, Kurzepa J, Biala G. Mephedrone and nicotine: oxidative stress and behavioral interactions in animal models. Neurochem Res 2015;40: 1083-93.

Avgustinovich DF, Kovalenko IL. [Long-term isolated housing causes anxiety in C57BL/6J female mice]. Ross Fiziol Zh Im I M Sechenova 2004;90: 351-60.

Ma XC, Jiang D, Jiang WH, Wang F, Jia M, Wu J, et al. Social isolation-induced aggression potentiates anxiety and depressive-like behavior in male mice subjected to unpredictable chronic mild stress. PLoS One 2011;6: e20955.

Hostetler CM, Anacker AM, Loftis JM, Ryabinin AE. Social housing and alcohol drinking in male-female pairs of prairie voles (Microtus ochrogaster). Psychopharmacology (Berl) 2012;224: 121-32.

Tramullas M, Dinan TG, Cryan JF. Chronic psychosocial stress induces visceral hyperalgesia in mice. Stress 2012;15: 281-92.

Nicholson A, Malcolm RD, Russ PL, Cough K, Touma C, Palme R, et al. The response of C57BL/6J and BALB/cJ mice to increased housing density. J Am Assoc Lab Anim Sci 2009;48: 740-53.

Ravenelle R, Santolucito HB, Byrnes EM, Byrnes JJ, Donaldson ST. Housing environment modulates physiological and behavioral responses to anxiogenic stimuli in trait anxiety male rats. Neuroscience 2014;270: 76-87.

Forsyth N, Young G, Mench J. Effects of cage size and enrichment on aggression and stereotypic behavior in 3 strains of laboratory mice. J Am Assoc Lab Anim Sci 2007;46: 93-94.

Thorpe JB, Gould KE, Borman ED, deCatanzaro D. Circulating and urinary adrenal corticosterone, progesterone, and estradiol in response to acute stress in female mice (Mus musculus). Horm Metab Res 2014;46: 211-8.

Weinhold LL, Ingersoll DW. Modulation of male mouse genital sniff, attack, and mount behaviors by urogenital substances from estrous females. Behav Neural Biol 1988;50: 207-28.

Ashokan A, Hegde A, Mitra R. Short-term environmental enrichment is sufficient to counter stress-induced anxiety and associated structural and molecular plasticity in basolateral amygdala. Psychoneuroendocrinology 2016;69: 189-96.

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IssueVol 15 No 1 (2020) QRcode
SectionOriginal Article(s)
DOI https://doi.org/10.18502/ijps.v15i1.2443
Keywords
Anxiety-Like Behavior Ovariectomized Mice Physical Enrichment Social Enrichment

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How to Cite
1.
Briones-Aranda A, Castellanos-Pérez M, Vega-Villa VM, Picazo O. Impact of Exposure to Environmental Enrichment on the Anxiety-Like Behavior of Ovariectomized Mice. Iran J Psychiatry. 2020;15(1):88-95.