Hostname: page-component-848d4c4894-r5zm4 Total loading time: 0 Render date: 2024-06-24T13:56:31.624Z Has data issue: false hasContentIssue false

Corticosterone differences rather than social housing predict performance of T-maze alternation in male CD-1 mice

Published online by Cambridge University Press:  01 January 2023

AE Fitchett
Affiliation:
Department of Psychology, Durham University, Science Site, South Road, Durham DH1 3LE, UK School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
CJ Barnard
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
HJ Cassaday*
Affiliation:
School of Psychology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
*
* Contact for correspondence and requests for reprints: helen.cassaday@nottingham.ac.uk

Abstract

This study examined the effects of social housing manipulations on bodyweight, corticosterone levels, and performance of T-maze alternation in male CD-1 mice. Males that adopted a dominant social rank were heavier than those that adopted a subordinate social rank. Dominant males also had lower corticosterone concentrations than the subordinates. However, there was little to suggest that these physiological indicators of social rank were moderated by housing condition. Indeed, statistical analysis confirmed that the difference in bodyweights was evident before males were socially housed. The mice showed high levels of spatial alternation on the T-maze from the start of testing so performance accuracy was high. Neither social rank nor housing condition had any clear categorical effect on T-maze performance. However, performance did fluctuate over successive blocks of testing and there was a negative association between accuracy on the T-maze and corticosterone levels (consistent with performance impairment because of elevated corticosterone). Therefore, under present conditions, individual differences in corticosterone were a better predictor of T-maze performance than social rank or housing condition. The results of the present study lend further support to the proposition that corticosterone levels measured non-invasively in urine may be used to predict diverse welfare outcomes for laboratory mice, from bodyweight to cognitive performance. Moreover, intrinsic physiological parameters rather than external influences, such as social housing, may have more influence on mouse behaviour.

Type
Research Article
Copyright
© 2009 Universities Federation for Animal Welfare

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andersson, M 1994 Sexual Selection. Princeton University Press: Princeton, New Jersey, USACrossRefGoogle Scholar
Avitsur, R, Stark, J and Sheridan, JF 2001 Social stress induces glucocorticoid resistance in subordinate animals. Hormones and Behavior 3: 247257CrossRefGoogle Scholar
Bakanova, LA, Druzin, MY, Kozlov, AP, Kurzina, NP and Malinina, EP 1997 The effects of proactive interference during spatial task performance in rats. Zhurnal Vysshei Nernoi Deiatelnosti Imeni IP Pavlova 4: 7885Google Scholar
Barnard, CJ and Luo, N 2002 Acquisition of dominance status affects maze learning in mice. Behavioural Processes 60: 5359CrossRefGoogle ScholarPubMed
Bartolomucci, A, Palanza, P, Gastani, L, Limiroli, E, Panerai, AE, Ceresini, G, Poli, MD and Parmigiani, S 2001 Social status in mice: Behavioral, endocrine and immune changes are context dependent. Physiology and Behavior 73: 401410CrossRefGoogle ScholarPubMed
Bartolomucci, A, Palanza, P, Sacerdote, P, Ceresini, G, Chirieleison, A, Panerai, AE and Parmigiani, S 2003a Individual housing induces altered immuno-endocrine responses to psychological stress in male mice. Psychoneuroendocrinology 2: 540558CrossRefGoogle Scholar
Bartolomucci, A, Palanza, P, Parmigiani, S, Pederzani, T, Merlot, E, Neveu, PJ and Dantzer, R 2003b Chronic psychosocial stress down-regulates central cytokines mRNA. Brain Research Bulletin 6: 173178CrossRefGoogle Scholar
Bartolomucci, A, Palanza, P, Costoli, C, Savani, E, Laviola, G, Parmigiani, S and Sgoifo, A 2003c Chronic psychosocial stress persistently affects autonomic function and physical activity in mice. Physiology and Behavior 80: 5767CrossRefGoogle Scholar
Bartolomucci, A, Pederzani, T, Sacerdote, P, Panerai, AE, Parmigiani, S and Palanza, P 2004 Behavioral and physiological characterisation of mice under chronic psychosocial stress. Psychoneuroendocrinology 29: 899910CrossRefGoogle Scholar
Bartolomucci, A, Palanza, P, Sacerdote, P, Panerai, AE, Sgoifo, A, Dantzer, R and Parmigiani, S 2005 Social factors and individual vulnerability to chronic stress exposure. Neuroscience and Biobehavioral Reviews 29: 6781CrossRefGoogle ScholarPubMed
Berton, O, McClung, CA, DiLeone, RJ, Krishnan, V, Renthal, W, Russo, SJ, Graham, D, Tsankova, NM, Bolanos, CA, Rios, M, Monteggia, LM, Self, DW and Nestler, EJ 2006 Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 31: 864868CrossRefGoogle Scholar
Blanchard, DC, Sakai, RR, McEwan, B, Weiss, SM and Blanchard, RJ 1993 Subordination stress: Behavioural, brain and neuroendocrine correlates. Behavioural Brain Research 5: 113121CrossRefGoogle Scholar
Brennan, FX, Ottenweller, JE, Seifu, Y, Zhu, G and Servatius, RJ 2000 Persistent stress-induced elevations of urinary corticosterone in rats. Physiology and Behavior 71: 441446Google ScholarPubMed
Buwalda, B, Kole, MHP, Veenema, AH, Huininga, M, de Boer, SF, Korte, SM and Koolhaas, JM 2005 Long-term effects of social stress on brain and behavior: A focus on hippocampal functioning. Neuroscience and Biobehavioral Reviews 2: 8397CrossRefGoogle Scholar
Cacho, R, Fano, E, Areso, P, Garmendia, L, Vegas, O, Brain, PF and Azpíroz, A 2003 Endocrine and lymphoproliferative response changes produced by social stress in mice. Physiology and Behavior 78: 505512CrossRefGoogle ScholarPubMed
Chida, Y, Sudo, N, Mori, J and Kubo, C 2006 Social isolation stress impairs passive avoidance learning in senescence-accelerated mouse (SAM). Brain Research 1067: 201208CrossRefGoogle Scholar
Clutton-Brock, TH, Albon, SD and Guinness, FE 1988 Reproductive success in male and female red deer. In: Clutton-Brock, TH (ed) Reproductive Success pp 325343. University of Chicago Press: Chicago, USAGoogle Scholar
Cohen, JS, Sturdy, C and Hicks, M 1996 Intratrial proactive interference in rats’ serial alternation performance in the radial maze. Animal Learning and Behavior 24: 300309CrossRefGoogle Scholar
Collins, SA, Gosling, LM, Hudson, J and Cowan, D 1997 Does behaviour after weaning affect the dominance status of adult male mice (Mus domesticus)? Behaviour 134: 9891002Google Scholar
Coudereau, JP, Debray, M, Monier, C, Bourre, JM and Frances, H 1997 Isolation impairs place preference conditioning to morphine but not aversive learning in mice. Psychopharmacology 130: 117123CrossRefGoogle Scholar
Crowcroft, P 1966 Mice All Over. Foulis: London, UKGoogle Scholar
Dahlborn, K, van Gils, BAA, van de Weerd, HA, van Dijk, JE and Baumans, V 1996 Evaluation of long-term environmental enrichment in the mouse. Scandinavian Journal of Laboratory Animal Science 23: 97106Google Scholar
De Jong, JG, van der Vegt, BJ, Buwalda, B and Koolhaas, JM 2005 Social environment determines the long-term effects of social defeat. Physiology and Behavior 84: 8795CrossRefGoogle ScholarPubMed
De Kloet, ER, Oitzl, MS and Joëls, M 1999 Stress and cognition: Are corticosteroids good or bad guys? Trends in Neurosciences 22: 422426CrossRefGoogle ScholarPubMed
De Kloet, ER, Grootendorst, J, Karssen, AM and Oitzl, MS 2002 Gene x environment interaction and cognitive performance: Animal studies on the role of corticosterone. Neurobiology of Learning and Memory 78: 570577CrossRefGoogle Scholar
De Kloet, ER, Joëls, M and Holsboer, F 2005 Stress and the brain: From adaptation to disease. Nature Reviews Neuroscience 6: 463475CrossRefGoogle ScholarPubMed
Desjardins, C, Maruniak, JA and Bronson, FH 1973 Social rank in house mice: Differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182: 939941CrossRefGoogle ScholarPubMed
Elliott, BM and Grunberg, NE 2005 Effects of social and physical enrichment on open field activity differ in male and female Sprague-Dawley rats. Behavioural Brain Research 165: 187196CrossRefGoogle ScholarPubMed
Faraday, MM 2002 Rat sex and strain differences in response to stress. Physiology and Behavior 75: 507522CrossRefGoogle Scholar
Fitchett, AE, Collins, SA, Barnard, CJ and Cassaday, HJ 2005a Subordinate male mice show long-lasting differences in spatial learning that persist when housed alone. Neurobiology of Learning and Memory 84: 247251CrossRefGoogle Scholar
Fitchett, AE, Collins, SA, Mason, H, Barnard, CJ and Cassaday, HJ 2005b Urinary corticosterone measures: Effects of strain and social rank in BKW and CD-1 mice. Behavioural Processes 70: 168176CrossRefGoogle Scholar
Fitchett, AE, Barnard, CJ and Cassaday, HJ 2006 There's no place like home: Cage odours and place preference in subordinate CD-1 male mice. Physiology and Behavior 87: 955962CrossRefGoogle ScholarPubMed
Gray, S and Hurst, JL 1995 The effects of cage cleaning on aggression within groups of male laboratory mice. Animal Behaviour 49: 821826CrossRefGoogle Scholar
Guo, M, Wu, CF, Liu, W, Yang, JY and Chen, D 2004 Sex difference in psychological behavior changes induced by long-term social isolation in mice. Progress in Neuro-Psychopharmacology and Biological Psychiatry 28: 115121CrossRefGoogle ScholarPubMed
Haseman, JK, Bourbina, J and Eustis, SL 1994 Effects of individual housing and other experimental design factors on tumor incidence in B6C3F1 mice. Fundamental and Applied Toxicology 23: 4452CrossRefGoogle ScholarPubMed
Hermes, GL, Jacobs, LF and McClintock, MK 2005 The sectored foraging field: A novel design to quantify spatial strategies, learning, memory, and emotion. Neurobiology of Learning and Memory 84: 6973CrossRefGoogle ScholarPubMed
Howell, DC 2002 Statistical Methods for Psychology, Fifth Edition. Duxbury Press: California, USAGoogle Scholar
Hurst, JL, Barnard, CJ, Nevison, CM and West, CD 1997 Housing and welfare in laboratory rats: Welfare implications of isolation and social contact among caged males. Animal Welfare 6: 329347Google Scholar
Ikemoto, S and Panksepp, J 1992 The effects of early social-isolation on the motivation for social play in juvenile rats. Developmental Psychobiology 25: 261274CrossRefGoogle ScholarPubMed
Jennings, M, Batchelor, GR, Brain, PF, Dick, A, Elliot, H, Francis, RJ, Hubrecht, RC, Hurst, JL, Morton, DB, Peters, AG, Raymond, R, Sales, GD, Sherwin, CM and West, C 1998 Refining rodent husbandry: The mouse. Report of the Rodent Refinement Working Party. Laboratory Animals 32: 233259CrossRefGoogle ScholarPubMed
Joëls, M, Karst, H, Alfarez, D, Heine, VM, Qin, Y, van Riel, E, Verkuyl, M, Lucassen, PJ and Krugers, HJ 2004 Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 7: 221231CrossRefGoogle ScholarPubMed
Joëls, M, Pu, Z, Wiegert, O, Oitzl, MS and Krugers, HJ 2006 Learning under stress: How does it work? Trends in Cognitive Sciences 10: 152158CrossRefGoogle ScholarPubMed
Keeney, AJ, Hogg, S and Marsden, CA 2001 Alterations in core body temperature, locomotor activity and corticosterone following acute and repeated social defeat of male NMRI mice. Physiology and Behavior 74: 177184CrossRefGoogle ScholarPubMed
Koolhaas, JM, Hermann, PM, Kemperman, C, Bohus, B, van den Hoofdakker, RH and Beersma, DGM 1990 Single social defeat in rats induces a gradual but long lasting behavioural change: A model of depression? Neuroscience Research Communications 7: 3541Google Scholar
Koolhaas, JM, De Boer, SF, De Ruiter, AJH, Meerlo, P and Sgoifo, A 1997 Social stress in rats and mice. Acta Physiologica Scandinavica 161(640): 6972Google Scholar
Koyama, S 1993 Isolation effect in mice (Mus musculus): Does it really induce aggression? Journal of Ethology 11: 117130CrossRefGoogle Scholar
Koyama, S 1995 Effects of a short period of isolation in adulthood on the aggressive behavior of dominant and subordinate male mice. Journal of Ethology 13: 175180CrossRefGoogle Scholar
Krohn, TC, Sorensen, DB, Ottesen, JL and Hansen, AK 2006 The effects of individual housing on mice and rats: a review. Animal Welfare 15: 343352Google Scholar
Kudryavtseva, NN, Bakshtanovskaya, IV and Koryakina, LA 1991 Social model of depression in mice of C57BL/6J strain. Pharmacology, Biochemistry and Behavior 38: 315320CrossRefGoogle ScholarPubMed
Lane, J 2006 Can non-invasive glucocorticoid measures be used as reliable indicators of stress in animals. Animal Welfare 15: 331342Google Scholar
Louch, CD and Higginbotham, M 1967 The relation between social rank and plasma corticosterone levels in mice. General Comparative Endocrinology 8: 441444CrossRefGoogle ScholarPubMed
Lu, L, Bao, G, Chen, H, Xia, P, Fan, X, Zhang, J, Pei, G and Ma, L 2003 Modification of hippocampal neurogenesis and neuroplasticity by social environments. Experimental Neurology 183: 600609CrossRefGoogle ScholarPubMed
Lucas, LR, Celen, Z, Tamashiro, KLK, Blanchard, RJ, Blanchard, DC, Markham, C, Sakai, RR and McEwen, BS 2004 Repeated exposure to social stress has long-term effects on indirect markers of dopaminergic activity in brain regions associated with motivated behaviour. Neuroscience 124: 449457CrossRefGoogle Scholar
Lumley, LA, Sipos, MI, Charles, RC, Charles, RF and Meyerhoff, JL 1999 Social stress effects on territorial marking and ultrasonic vocalizations in mice. Physiology and Behavior 67: 769775CrossRefGoogle ScholarPubMed
Mackintosh, JH 1981 Behaviour of the house mouse. Symposium of the Zoological Society of London 47: 337365Google Scholar
Martínez, M, Calvo-Torrent, A and Pico-Alfonso, MA 1998 Social defeat and subordination as models of social defeat in laboratory rodents: A review. Aggressive Behavior 24: 2412563.0.CO;2-M>CrossRefGoogle Scholar
McEwen, BS and Sapolsky, RM 1995 Stress and cognitive function. Current Opinion in Neurobiology 5: 205216CrossRefGoogle ScholarPubMed
McEwen, BS 2004 Protection and damage from acute and chronic stress: Allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Annals of the New York Academy of Sciences 1032: 17CrossRefGoogle Scholar
Meerlo, P, De Boer, SF, Koolhaas, JM, Daan, S and van den Hoofdakker, RH 1996a Changes in daily rhythms of body temperature and activity after a single social defeat in rats. Physiology and Behavior 59: 735739CrossRefGoogle Scholar
Meerlo, P, Overkamp, GJF, Benning, MA, Koolhaas, JM and van Den Hoofdakker, RH 1996b Long-term changes in open field behaviour following a single social defeat in rats can be reversed by sleep deprivation. Physiology and Behavior 60: 115119CrossRefGoogle Scholar
Meerlo, P, Overkamp, GJF, Daan, S, van den Hoofdakker, RH and Koolhaas, JM 1996c Changes in behaviour and body weight following a single or double social defeat. Stress 1: 2132CrossRefGoogle Scholar
Mondragón, R, Mayagoitia, L, López-Luján, A and Díaz, J 1987 Social structure features in three inbred strains of mice, C57B1/6J, Balb/cj, and NIH: A comparative study. Behavioral and Neural Biology 47: 384391Google Scholar
Moragrega, I, Carrasco, MC, Vicens, P and Redolat, R 2003 Spatial learning in male mice with different levels of aggressiveness: Effects of housing conditions and nicotine administration. Behavioural Brain Research 147: 18CrossRefGoogle ScholarPubMed
Moragrega, I, Carrasco, MC and Redolat, R 2005 Effects of housing and nicotine on shuttle-box avoidance in male NMRI mice. Behavioural Brain Research 164: 178187CrossRefGoogle ScholarPubMed
Muir, C, Spironella-Vella, E, Pisani, N and De Catanzaro, D 2001 Enzyme immunoassay of 17 beta-estradiol, estrone conjugates, and testosterone in urinary and fecal samples from male and female mice. Hormone and Metabolic Research 33: 653658CrossRefGoogle ScholarPubMed
Poole, TB and Morgan, HDR 1973 Differences in aggressive behaviour between male mice (Mus musculus L.) in colonies of different sizes. Animal Behaviour 21: 788795CrossRefGoogle ScholarPubMed
Poole, TB and Morgan, HDR 1976 Social and territorial behaviour of laboratory mice (Mus musculus L.) in small complex areas. Animal Behaviour 24: 476480CrossRefGoogle Scholar
Ruis, MAW, Brake, JHA, Buwalda, B, De Boer, SF, Meerlo, P, Korte, SM, Blokhuis, HJ and Koolhaas, JM 1999 Housing familiar male wild-type rats together reduces the long-term adverse behavioural and physiological effects of social stress. Psychoneuroendocrinology 24: 285300CrossRefGoogle Scholar
Sandstrom, NJ and Hart, SR 2005 Isolation stress during the third postnatal week alters radial arm maze performance and corticosterone levels in adulthood. Behavioural Brain Research 156: 289296CrossRefGoogle ScholarPubMed
Sapolsky, RM 1999 Glucocorticoids, stress, and their adverse neurological effects: Relevance to aging. Experimental Gerontology 34: 721732CrossRefGoogle ScholarPubMed
Schüler, L and Renne, U 1988 Relationship of social rank in mice to growth, endurance, and fertility. Aggressive Behaviour 14: 2052113.0.CO;2-J>CrossRefGoogle Scholar
Schulkin, J 1999 The Neuroendocrine Regulation of Behaviour. Cambridge University Press: Cambridge, UKGoogle Scholar
Sloman, KA, Montpetit, CJ and Gilmour, KM 2002 Modulation of catecholamine release and cortisol secretion by social interactions in the rainbow trout, Oncorhynchus mykiss. General and Comparative Endocrinology 127: 136146CrossRefGoogle ScholarPubMed
Spritzer, MD, Meikle, DB and Solomon, NG 2004 The relationship between rank and spatial ability among male meadow voles (Microtus pennsylvanicus). Journal of Comparative Psychology 118: 332339CrossRefGoogle Scholar
Suckow, MA, Dannerman, P and Brayton, C 2001 The Laboratory Mouse. CRC Press LLC: Florida, USAGoogle Scholar
Summers, CH, Summers, TR, Moore, MC, Korzan, WJ, Woodley, SK, Ronan, PJ, Hoglund, E, Watt, MJ and Greenberg, N 2003 Temporal patterns of limbic monoamine and plasma corticosterone response during social stress. Neuroscience 116: 553563CrossRefGoogle ScholarPubMed
Tornatzky, W and Miczek, KA 1993 Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiology Behaviour 53: 983993CrossRefGoogle ScholarPubMed
Touma, C, Sachser, N, Möstl, E and Palme, R 2003 Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. General and Comparative Endocrinology 130: 267278CrossRefGoogle ScholarPubMed
Valzelli, L 1973 The “Isolation Syndrome” in mice. Psychopharmacologia 31: 305320CrossRefGoogle ScholarPubMed
Valzelli, L, Bernasconi, S and Cusumano, G 1977 Prolonged isolation and alcohol effect on avoidance learning in two strains of mice. Neuropsychobiology 3: 135143CrossRefGoogle ScholarPubMed
van Loo, PLP, Kruitwagon, CLJJ, van Zutphen, LFM, Koolhaas, JM and Baumans, V 2000 Modulation of aggression in male mice: Influence of cage cleaning regime and scent marks. Animal Welfare 9: 281295Google Scholar
van Loo, PLP, Mol, JA, Koolhaas, JM, van Zutphen, BFM and Baumans, V 2001a Modulation of aggression in male mice: Influence of group size and cage size. Physiology and Behaviour 72: 675683CrossRefGoogle Scholar
van Loo, PLP, De Groot, AC, van Zutphen, LFM and Baumans, V 2001b Do male mice prefer or avoid each other's company? - Influence of hierarchy, kinship and familiarity. Journal of Applied Animal Welfare Science 4: 91103CrossRefGoogle Scholar
van Loo, PLP, Kruitwagen, CLJJ, Koolhaas, JM, van de Weerd, HA, van Zutphen, LFM and Baumans, V 2002 Influence of cage enrichment on aggressive behaviour and physiological parameters in male mice. Applied Animal Behaviour Science 76: 6581CrossRefGoogle Scholar
van Loo, PLP, van Der Meer, E, Kruitwagen, CLJJ, Koolhaas, JM, van Zutphen, LFM and Baumans, V 2003 Strain-specific aggressive behaviour of male mice submitted to different husbandry procedures. Aggressive Behaviour 29: 6980CrossRefGoogle Scholar
van Loo, PLP, van de Weerd, HA, van Zutphen, LFM and Baumans, V 2004 Preference for social contact versus environmental enrichment in male laboratory mice. Laboratory Animals 38: 178188CrossRefGoogle ScholarPubMed
van Zegeren, K 1980 Variation in aggressiveness and the regulation of numbers in house mouse populations. Netherlands Journal of Zoology 30: 635770CrossRefGoogle Scholar
Wittenberger, JF 1981 Animal Social Behavior. Wadsworth Inc: California, USAGoogle Scholar
Wongwitdecha, N and Marsden, CA 1996 Social isolation increases aggressive behaviour and alters the effects of diazepam in the rat social interaction test. Behavioural Brain Research 75: 2732CrossRefGoogle ScholarPubMed
Wu, W, Yamaura, T, Murakami, K, Murata, J, Matsumoto, K, Watanabe, H and Saiki, I 2000 Social isolation stress enhanced liver metastasis of murine colon 26-L5 carcinoma cells by suppressing immune responses in mice. Life Sciences 66: 18271838CrossRefGoogle ScholarPubMed