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The effects of individual housing on mice and rats: a review

Published online by Cambridge University Press:  11 January 2023

TC Krohn ,
DB Sørensen ,
JL Ottesen  and
AK Hansen
TC Krohn*
Affiliation:
The Royal Veterinary and Agricultural University, Centre for Applied Laboratory Animal Research, Laboratory Animal Science and Welfare, Dept. of Veterinary Pathobiology, Groennegaardsvej 15, DK-1870 Frederiksberg C, Denmark
DB Sørensen
Affiliation:
The Royal Veterinary and Agricultural University, Centre for Applied Laboratory Animal Research, Laboratory Animal Science and Welfare, Dept. of Veterinary Pathobiology, Groennegaardsvej 15, DK-1870 Frederiksberg C, Denmark
JL Ottesen
Affiliation:
Novo Nordisk A/S, Centre for Applied Laboratory Animal Research, DK-2760 Måløv, Denmark
AK Hansen
Affiliation:
The Royal Veterinary and Agricultural University, Centre for Applied Laboratory Animal Research, Laboratory Animal Science and Welfare, Dept. of Veterinary Pathobiology, Groennegaardsvej 15, DK-1870 Frederiksberg C, Denmark
*
* Contact for correspondence and request for reprints: tkr@kvl.dk
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Abstract

Isolating an animal refers to the situation where the animal is physically fully demarcated from conspecifics without physical, visual, olfactory and auditory contact. Animals housed in separate cages in the same room are, although deprived of physical and visual contact, still in olfactory and auditory contact, and thus not totally isolated. During the fifties and sixties several studies claimed to show physiological and behavioural differences between individually and group housed rats and mice. The so-called ‘Isolation Syndrome’ characterised by changes in corticosterone levels, metabolism, growth, and behaviour was introduced, rather as a model for psychoneurosis than through any concern for animal welfare. Today, it is often stated as common knowledge in laboratory animal science textbooks that individual housing as well as isolation of rats and mice has an effect on physiology and behaviour. It is, however, unclear whether this effect actually impairs animal welfare.

The aim of this paper is to analyse studies on individual housing of mice and rats to evaluate whether there is documented proof that individual housing affects welfare, and, alternatively whether it is possible to house these animals individually without negative impact on welfare, eg by providing special housing improvements.

A range of studies have shown that individual housing or isolation has effects on corticosterone, the open field behaviour, barbiturate sleeping time and the metabolism of different pharmaceuticals in the animals. However, this review of 37 studies in rats and 17 studies in mice showed divergence in test results difficult to explain, as many studies lacked basal information about the study, eg information on genetic strains and housing conditions, such as bedding, enrichment and cage sizes. Furthermore, test and control groups most frequently differed in cage sizes and stocking densities, and behavioural tests differed in ways which may very well explain the differences in results. Overall, there seemed to be an effect of individual housing, although it may be small, and it seems reasonable to assume that, through making small changes in the procedures and housing environments, the effects can be minimised or even eliminated. More well-controlled and standardised studies are needed to give more specific answers to the questions this issue poses.

Keywords

animal welfareindividual housingisolationmicerats
Type
Research Article
Information
Animal Welfare , Volume 15 , Issue 4 , November 2006 , pp. 343 - 352
Copyright
© 2006 Universities Federation for Animal Welfare

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References

Adolph, EF 1947 Urges to eat and drink in rats. American Journal of Physiology 151: 110–125CrossRefGoogle ScholarPubMed
Baenninger, LP 1967 Comparison of behavioural development in socially isolated and grouped rats. Animal Behaviour 15: 312–323CrossRefGoogle ScholarPubMed
Baer, H 1971 Long-term isolation stress and its effects on drug response in rodents. Laboratory Animal Science 21: 341–349Google ScholarPubMed
Barnett, JL, Dickson, RG and Hocking, WE 1979 Genotype and environment in the social interactions of wild and domestic “norway” rats. Aggressive Behavior 5: 105–1193.0.CO;2-U>CrossRefGoogle Scholar
Barnett, SA and Cowan, PE 1976 Activity, exploration, curiosity and fear: an ethological study. Interdisciplinary Science Reviews 1: 43–62CrossRefGoogle Scholar
Baumans, V 1999 The laboratory mouse. In: Poole T (ed.) The UFAW Handbook on the care and management of laboratory animals pp 282–312. Blackwell Science: Oxford, UKGoogle Scholar
Benton, D and Brain, PF 1979 Behavioral comparisons of isolated, dominant and subordinate mice. Behavioural Processes 4: 211–219CrossRefGoogle ScholarPubMed
Benton, D and Brain, PF 1981 Behavioral and adrenocortical reactivity in female mice following individual or group housing. Developmental Psychobiology 14: 101–107CrossRefGoogle ScholarPubMed
Berdoy, M 2002 The laboratory rat: A natural history. DVD, Oxford University, UK: http://www.ratlife.orgGoogle Scholar
Berry, RJ 1970 The natural history of the house mouse. Field Studies 3: 219–262Google Scholar
Blom, HJM 1993 Evaluation of housing conditions for laboratory mice and rats - The use of preference tests for studying choice behaviour. PhD Thesis, The University of Utrecht, The NetherlandsGoogle Scholar
Brain, P 1975 What does individual housing mean to a mouse? Life Sciences 16: 187–200CrossRefGoogle ScholarPubMed
Brain, P 1989 Social stress in laboratory mouse colonies. In: Poole, TB (ed) Laboratory Animal Welfare Research pp 49–61. Universities Federation for Animal Welfare: Wheathampstead, Herts, UKGoogle Scholar
Brain, P 1992 Understanding the behaviours of feral species may facilitate design of optimal living conditions for common laboratory rodents. Animal Technology 43: 99–105Google Scholar
Broom, DM and Johnson, KG 1993 Stress and animal welfare. Chapman & Hall: London, UKCrossRefGoogle Scholar
Brown, KJ and Grunberg, NE 1995 Effects of housing on male and female rats: crowding stresses male but calm females. Physiology & Behavior 58: 1085–1089CrossRefGoogle ScholarPubMed
Brown, KJ and Grunberg, NE 1996 Effects of environmental conditions on food consumption in female and male rats. Physiology & Behavior 60: 293–297CrossRefGoogle ScholarPubMed
Cairns, RB, Hood, KE and Midlam, J 1985 On fighting in mice - Is there a sensitive period for isolation effects. Animal Behaviour 33: 166–180CrossRefGoogle Scholar
Calhoun, JB 1962 The ecology and sociology of the Norway rat. US Department of Health, Education, and Welfare. Public Health Service: Baltimore, USAGoogle Scholar
Crawley, JN 2000 What's wrong with my mouse? Wiley-Liss: New York, USAGoogle Scholar
Cunliffe-Beamer, TL, Freeman, LC and Myers, DD 1981 Barbiturate sleeptime in mice exposed to autoclaved or unauto-claved wood beddings. Laboratory Animal Science 31: 672–675Google ScholarPubMed
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: 97–106Google Scholar
Dairman, W and Balazs, T 1970 Comparison of liver micro-some enzyme systems and barbiturate sleep times in rats caged individually or communally. Biochemical Pharmacology 19: 951–955CrossRefGoogle ScholarPubMed
Dalrymple-Alford, JC and Benton, D 1981a The effect of social isolation of the rat on open-field activity and emergence. Behavioral Processes 6: 283–290CrossRefGoogle ScholarPubMed
Dalrymple-Alford, JC and Benton, D 1981b Activity differences of individually and group housed male and female rats. Animal Learning & Behavior 9: 50–55CrossRefGoogle Scholar
de Catanzaro, D and Gorzalka, BB 1980 Sexual arousal in male mice: effects of brief periods of isolation or grouping. Behavioral and Neural Biology 28: 442–453Google ScholarPubMed
Einon, D, Stewart, J, Atkinson, S and Morgan, M 1976 Effect of isolation on barbiturate anaesthesia in the rat. Psychopharmacology 50: 85–88Google ScholarPubMed
Einon, DF, Humphreys, AP, Chivers, SM, Field, S and Naylor, V 1981 Isolation has permanent effects upon the behavior of the rat, but not the mouse, gerbil, or guinea pig. Developmental Psychobiology 14: 343–355Google ScholarPubMed
Eskola, S and Kaliste-Korhonen, E 1998 Nesting material and number of females per cage: effects on mouse productivity in BALB/c, C57BL/6J, DBA/2 and NIH/S mice. Laboratory Animals 33: 122–128CrossRefGoogle Scholar
Faggin, BM and Palermo-Neto, J 1985 Differential alterations in brain sensitivity to amphetamine and pentylenetetrazol in socially deprived mice. General Pharmacology 16: 299–302CrossRefGoogle ScholarPubMed
File, SE 1978 Exploration, distraction, and habituation in rats reared in isolation. Developmental Psychobiology 11: 73–81CrossRefGoogle ScholarPubMed
File, SE and Vellucci, SV 1979 Behavioral and biochemical measures of stress in hooded rats from different sources. Physiology & Behavior 22: 31–35CrossRefGoogle ScholarPubMed
Gamallo, A, Villanua, A, Trancho, G and Fraile, A 1986 Stress adaptation and adrenal activity in isolated and crowded rats. Physiology & Behavior 36: 217–221Google ScholarPubMed
Gentsch, C, Lichtsteiner, M and Feer, H 1981 Locomotor activity, defecation score and corticosterone levels during an openfield exposure: a comparison among individually and group-housed rats, and genetically selected rat lines. Physiology & Behavior 27: 183–186CrossRefGoogle ScholarPubMed
Gentsch, C, Lichtsteiner, M, Kraeuchi, K and Feer, H 1982 Different reaction patterns in individually and socially reared rats during exposures to novel environments. Behavioural and Brain Research 4: 45–54CrossRefGoogle ScholarPubMed
Goldsmith, JF, Brain, PF and Benton, D 1978 Effects of the duration of individual or group housing on behavioural and adrenocortical reactivity in male mice. Physiology & Behavior 21: 757–760CrossRefGoogle ScholarPubMed
Gosling, LM, Atkinson, NW, Dunn, S and Collins, SA 1996 The response of subordinate male mice to scent marks varies in relation to their own competitive ability. Animal Behaviour 52: 1185–1191CrossRefGoogle Scholar
Greco, AM, Gambardella, P, Sticchi, R, D'Aponte, D, Di Renzo, G and de Franciscis, P 1989 Effects of individual housing on circadian rhythms of adult rats. Physiology & Behavior 45: 363–366Google ScholarPubMed
Hall, FS, Huang, S, Fong, GW, Sundstrom, JM and Pert, A 2000 Differential basis of strain and rearing effects on open-field behavior in Fawn Hooded and Wistar rats. Physiology & Behavior 71: 525–532CrossRefGoogle ScholarPubMed
Hall, FS, Humby, T, Wilkinson, LS and Robbins, TW 1997a The effects of isolation rearing on preference by rats for a novel environment. Physiology & Behavior 62: 281–290CrossRefGoogle ScholarPubMed
Hall, FS, Humby, T, Wilkinson, LS and Robbins, TW 1997b The effects of isolation rearing of rats on behavioural responses to food and environmental novelty. Physiology & Behavior 62: 299–303CrossRefGoogle ScholarPubMed
Hallback, M 1975 Consequence of social isolation on blood pressure, cardiovascular reactivity and design in spontaneously hypertensive rats. Acta Physiologica Scandinavica 93: 455–465CrossRefGoogle ScholarPubMed
Hatch, AM, Wiberg, GS, Zawidzka, Z, Cann, M, Airth, JM and Grice, HC 1965 Isolation syndrome in rat. Toxicology and Applied Pharmacology 7: 737–745CrossRefGoogle Scholar
Hayes, LD 2000 To nest communally or not to nest communally: a review of rodent communal nesting and nursing. Animal Behaviour 59: 677–688CrossRefGoogle ScholarPubMed
Heidbreder, CA, Weiss, IC, Domeney, AM, Pryce, C, Homberg, J, Hedou, G, Feldon, J, Moran, MC and Nelson, P 2000 Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome. Neuroscience 100: 749–768CrossRefGoogle ScholarPubMed
Holmes, A, Parmigiani, S, Ferrari, PF, Palanza, P and Rodgers, RJ 2000 Behavioral profile of wild mice in the elevated plus-maze test for anxiety. Physiology & Behavior 71: 509–516CrossRefGoogle ScholarPubMed
Holson, RR, Scallet, AC, Ali, SF, Sullivan, P and Gough, B 1988 Adrenocortical, β-endorphin and behavioral responses to graded stressors in differentially reared rats. Physiology & Behavior 42: 125–130CrossRefGoogle ScholarPubMed
Holson, RR, Scallet, AC, Ali, SF and Turner, BB 1991 Isolation stress revisited: Isolation rearing effects depend on animal care methods. Physiology & Behavior 49: 1107–1118CrossRefGoogle ScholarPubMed
Hurst, JL 1990 Urine marking in populations of wild house mice (Mus domesticus rutty): 1, Communication between males. Animal Behaviour 40: 209–222CrossRefGoogle 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: 329–347CrossRefGoogle Scholar
Hurst, JL, Barnard, CJ, Nevison, CM and West, CD 1998 Housing and welfare in laboratory rats: the welfare implications of social isolation and social contact among females. Animal Welfare 7: 121–136CrossRefGoogle Scholar
Hurst, JL, Payne, CE, Nevison, CM, Marie, AD, Humphries, RE, Robertson, DHL, Cavaggioni, A and Beynon, RJ 2001 Individual recognition in mice mediated by major urinary proteins. Nature 414: 631–634CrossRefGoogle ScholarPubMed
Koolhaas, JM 1999 The laboratory rat. In: Poole, T (ed) The UFAW Handbook on the care and management of laboratory animals pp 313–330. Blackwell Science: Oxford, UKGoogle Scholar
Kostowski, W, Czlonkowski, A, Rewerski, W and Piechocki, T 1977 Morphine action in grouped and isolated rats and mice. Psychopharmacology 53: 191–193CrossRefGoogle ScholarPubMed
Krohn, TC and Hansen, AK 2001 Weighing as automatic registration of preferences when testing rats. Scandinavian Journal of Laboratory Animal Science 28: 223–229Google Scholar
Krohn, TC and Hansen, AK 2002 The application of traditional behavioural and physiological methods for monitoring of the welfare impact of different flooring conditions in rodents. Scandinavian Journal of Laboratory Animal Science 29: 79–89Google Scholar
Krohn, TC, Hansen, AK and Dragsted, N 2003 Telemetry as a method for measuring impacts of housing conditions on rats. Animal Welfare 12: 53–62CrossRefGoogle Scholar
Latham, N and Mason, G 2004 From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory. Applied Animal Behaviour Science 86: 261–289Google Scholar
Les, EP 1968 Cage population density and efficiency of feed utilization in inbred mice. Laboratory Animal Care 18: 305–313Google ScholarPubMed
Lore, R and Flannelly, K 1977 Rat societies. Scientific American 236: 106–116CrossRefGoogle ScholarPubMed
Lovell, DP 1986a Variation in pentobarbitone sleeping time in mice. (1) Strain and sex differences. Laboratory Animals 20: 85–90CrossRefGoogle ScholarPubMed
Lovell, DP 1986b Variation in barbiturate sleeping time in mice. (3) Strain × environment interaction. Laboratory Animals 20: 307–312CrossRefGoogle Scholar
Mackintosh, JH 1973 Factors affecting recognition of territory boundaries by mice (Mus musculus). Animal Behaviour 21: 464–470CrossRefGoogle Scholar
Manning, CJ, Dewsbury, DA, Wakeland, EK and Potts, WK 1995 Communal nesting and communal nursing in house mice, Mus musculus domesticus. Animal Behaviour 50: 741–751CrossRefGoogle Scholar
Manosevitz, M and Pryor, JB 1975 Cage size as a factor in environmental enrichment. Journal of Comparative and Physiological Psychology 89: 648–654CrossRefGoogle Scholar
Manser, CE, Elliott, H, Morris, TH, and Broom, DM 1996 The use of a novel operant test to determine the strength of preference for flooring in laboratory rats. Laboratory Animals 30: 1–6CrossRefGoogle ScholarPubMed
McGlone, JJ, Anderson, DL and Norman, RL 2001 Floor space needs for laboratory mice: BALB/cJ males or females in solid-bottom cages with bedding. Contemporary Topics In Laboratory Animal Science 40: 21–25Google ScholarPubMed
Meikle, DB, Kruper, JH and Browning, CR 1995 Adult male house mice born to undernourished mothers are unattractive to oestrous females. Animal Behaviour 50: 753–758CrossRefGoogle Scholar
Misslin, R, Herzog, F, Koch, B and Ropartz, P 1982 Effects of isolation, handling and novelty on the pituitary-adrenal response in the mouse. Psychoneuroendocrinology 7: 217–221CrossRefGoogle ScholarPubMed
Mohammed, AH, Zhu, SW, Darmopil, S, Hjerling-Leffler, J, Ernfors, P, Winblad, B, Diamond, MC, Eriksson, PS and Bogdanovic, N 2002 Environmental enrichment and the brain. Progress in Brain Research 138: 109–133CrossRefGoogle ScholarPubMed
Nabeshima, T and Ho, IK 1981 Pharmacological responses to pentobarbital in different strains of mice. Journal of Pharmacology and Experimental Therapeutics 216: 198–204Google ScholarPubMed
Nagy, TR, Krzywanski, D, Li, J, Meleth, S and Desmond, R 2002 Effect of group vs single housing on phenotypic variance in C57BL/6J mice. Obesity Research 10: 412–415CrossRefGoogle ScholarPubMed
Niesink, RJ and van Ree, JM 1982 Short-term isolation increases social interactions of male rats: a parametric analysis. Physiology & Behavior 29: 819–825CrossRefGoogle ScholarPubMed
Nowak, RM 1999 Walker's Mammals of the world. The John Hopkins University Press: Baltimore, USAGoogle Scholar
O'Connor, R and Eikelboom, R 2000 The effects of changes in housing on feeding and wheel running. Physiology & Behavior 68: 361–371CrossRefGoogle ScholarPubMed
Ödberg, FO 1984 Neurochemical correlates of stereotyped behavior in voles. Applied Animal Behaviour Science 13: 168CrossRefGoogle Scholar
Ödberg, FO 1987 The influence of cage size and environmental enrichment on the development of stereotypies in bank voles (Clethrionomys glareolus). Behavioral Processes 14: 155–173CrossRefGoogle ScholarPubMed
Ödberg, FO, Kennes, D, Derycke, PH and Bouquet, Y 1987 The effect of interference in catecholamine biosynthesis on captivity induced jumping stereotypy in bank voles (Clethrionomys glareolus). Archives Internationales de Pharmacodynamie et de Therapie 285: 34–42Google ScholarPubMed
Patterson-Kane, EG, Harper, DN and Hunt, M 2001 The cage preferences of laboratory rats. Laboratory Animals 35: 74–79CrossRefGoogle ScholarPubMed
Peng, X, Lang, CM, Drozdowitz, CK and Ohlsson-Wilhelm, BM 1989 Effect of cage population density on plasma corticos-terone and peripheral lymphocyte populations of laboratory mice. Laboratory Animals 23: 302–306CrossRefGoogle ScholarPubMed
Pérez, C, Canal, JR, Domínguez, E, Campillo, JE, Guillén, M and Torres, MD 1997 Individual housing influences certain biochemical parameters in the rat. Laboratory Animals 31: 357–361CrossRefGoogle ScholarPubMed
Plaut, SM and Grota, LJ 1971 Effects of differential housing on adrenocortical reactivity. Neuroendocrinology 7: 348–360CrossRefGoogle ScholarPubMed
Poole, TB and Morgan, HDR 1973 Differences in aggressive behavior between male mice (Mus musculus L) in colonies of different sizes. Animal Behaviour 21: 788–795CrossRefGoogle ScholarPubMed
Poole, TB and Morgan, HDR 1976 Social and territorial behavior of laboratory mice (Mus musculus L) in small complex areas. Animal Behaviour 24: 476–480CrossRefGoogle Scholar
Puglisi-Allegra, S and Oliverio, A 1983 Social isolation - Effects on pain threshold and stress induced analgesia. Pharmacology Biochemistry and Behavior 19: 679–681CrossRefGoogle ScholarPubMed
Robbins, TW, Jones, GH and Wilkinson, LS 1996 Behavioural and neurochemical effects of early social deprivation in the rat. Journal of Psychopharmacology 10: 39–47CrossRefGoogle ScholarPubMed
Rodgers, RJ and Cole, JC 1993 Influence of social isolation, gender, strain, and prior novelty on plus maze behavior in mice. Physiology & Behavior 54: 729–736CrossRefGoogle Scholar
Sachser, N and Kaiser, S 1997 The social environment, behaviour and stress - a case study in guinea pigs. Acta Physiologica Scandinavica Supplementum 640: 83–87Google Scholar
Sahakian, BJ, Robbins, TW and Iversen, SD 1977 Effects of isolation rearing on exploration in rat. Animal Learning & Behavior 5: 193–198CrossRefGoogle Scholar
Sales, GD and Milligan, SR 1992 Ultrasound and laboratory animals. Animal Technology 43: 89–98Google Scholar
Schenk, S, Hunt, T, Klukowski, G and Amit, Z 1987 Isolation housing decreases the effectiveness of morphine in the conditioned taste aversion paradigm. Psychopharmacology 92: 48–51CrossRefGoogle ScholarPubMed
Schenk, S, Robinson, B and Amit, Z 1988 Housing conditions fail to affect the intravenous self-administration of amphetamine. Pharmacology Biochemistry and Behavior 31: 59–62CrossRefGoogle ScholarPubMed
Schmitt, U and Hiemke, C 1998 Strain differences in open-field and elevated plus-maze behavior of rats without and with pretest handling. Pharmacology Biochemistry & Behavior 59: 807–811CrossRefGoogle ScholarPubMed
Schrijver, NCA, Bahr, NI, Weiss, IC and Würbel, H 2002 Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacology Biochemistry and Behavior 73: 209–224CrossRefGoogle ScholarPubMed
Sharp, J, Zammit, T, Azar, T and Lawson, D 2003 Stress-like responses to common procedures in individually and group-housed female rats. Contemporary Topics In Laboratory Animal Science 42: 9–18Google ScholarPubMed
Sherwin, CM 1996 Laboratory mice persist in gaining access to resources: A method of assessing the importance of environmental features. Applied Animal Behaviour Science 48: 203–213CrossRefGoogle Scholar
Sherwin, CM and Nicol, CJ 1996 Reorganization of behaviour in laboratory mice, Mus musculus, with varying cost of access to resources. Animal Behaviour 51: 1087–1093CrossRefGoogle Scholar
Sluyter, F and van Oortmerssen, GA 2000 A mouse is not just a mouse. Animal Welfare 9: 193–205CrossRefGoogle Scholar
Smith, J, Hurst, JL and Barnard, CJ 1994 Comparing behaviour in wild and laboratory strains of the house mouse: Levels of comparison and functional inference. Behavioural Processes 32: 79–86CrossRefGoogle ScholarPubMed
Sobel, EH, Zuppinger, KA and Joss, EE 1979 Effects of isolation, handling and restraint on growth of rats. Growth 43: 1–6Google ScholarPubMed
Spani, D, Arras, M, König, B and Rülicke, T 2003 Higher heart rate of laboratory mice housed individually vs in pairs. Laboratory Animals 37: 54–62CrossRefGoogle ScholarPubMed
Stanford, SC, Parker, V and Morinan, A 1988 Deficits in exploratory behavior in socially isolated rats are not accompanied by changes in cerebral cortical adrenoceptor binding. Journal of Affective Disorders 15: 175–180CrossRefGoogle Scholar
Steiner, H and Gerfen, CR 1998 Role of dynorphin and enkephalin in the regulation of striatal output pathways and behavior. Experimental Brain Research 123: 60–76CrossRefGoogle ScholarPubMed
Stern, JA, Winokur, G, Eisenstein, A, Taylor, R and Sly, M 1960 The effect of group vs individual housing on behavior and physiological responses to stress in the albino rat. Journal of Psychosomatic Research 4: 185–190CrossRefGoogle ScholarPubMed
Svendsen, P 1994 Environmental impact on animal experiments. In: Svendsen, P and Hau, J (eds) Handbook of Laboratory Animal Science pp 191–202. CRC Press Inc: Boca Raton, Florida, USAGoogle Scholar
Swanson, HH and van de Poll, NE 1983 Effects of an isolated or enriched environment after handling on sexual maturation and behaviour in male and female rats. Journal of Reproduction and Fertility 69: 165–171CrossRefGoogle ScholarPubMed
Syme, LA and Hughes, RN 1972 Social isolation in young rats - Effects of cage size on open field behavior. Psychonomic Science 29: 25–26CrossRefGoogle Scholar
Szenasi, G, Bencsath, P and Takacs, L 1988 No Effect of isolation on blood pressure and daily electrolyte excretion in rats. Acta Physiologica Hungarica 72: 93–98Google ScholarPubMed
Takemoto, TI, Suzuki, T and Miyama, T 1975 Effects of isolation on mice in relation to age and sex. Tohoku Journal of Experimental Medicine 117: 153–165CrossRefGoogle ScholarPubMed
Thiessen, DD 1966 Relation of social position and wounding to exploratory behavior and organ weights in house mice. Journal of Mammalogy 47: 28–34CrossRefGoogle ScholarPubMed
Tuli, JS, Smith, JA and Morton, DB 1995 Corticosterone, adrenal and spleen weight in mice after tail bleeding, and its effect on nearby animals. Laboratory Animals 29: 90–95CrossRefGoogle ScholarPubMed
Vadiei, K, Berens, KL and Luke, DR 1990 Isolation induced renal functional changes in rats from 4 breeders. Laboratory Animal Science 40: 56–59Google ScholarPubMed
Valzelli, L 1973 Isolation syndrome in mice. Psychopharmacologia 31: 305–320CrossRefGoogle ScholarPubMed
van de Weerd, HA, Baumans, V, Koolhaas, JM and van Zutphen, LFM 1994 Strain specific behavioural response to environmental enrichment in the mouse. Journal of Experimental Animal Science 36: 117–127Google ScholarPubMed
van den Berg, CL, van Ree, JM and Spruijt, BM 1999 Sequential analysis of juvenile isolation-induced decreased social behavior in the adult rat. Physiology & Behavior 67: 483–488CrossRefGoogle ScholarPubMed
van Loo, PL, Mol, JA, Koolhaas, JM, van Zutphen, BF and Baumans, V 2001 Modulation of aggression in male mice: influence of group size and cage size. Physiology & Behavior 72: 675–683CrossRefGoogle ScholarPubMed
Viveros, MP, Hernández, R, Martínez, I and González, P 1990 Effects of social isolation and crowding upon adrenocortical reactivity and behaviour in the rat. Animal Learning & Behavior 18: 90–96CrossRefGoogle Scholar
Walsh, RN and Cummins, RA 1976 The Open-Field Test: A critical review. Psychological Bulletin 83: 482–504CrossRefGoogle ScholarPubMed
Watanabe, H, Ohdo, S, Ishikawa, M and Ogawa, N 1992 Effects of social isolation on pentobarbital activity in mice: relationship to racemate levels and enantiomer levels in brain. Journal of Pharmacology and Experimental Therapeutics 263: 1036–1045Google ScholarPubMed
Weltman, AS, Sackler, AM, Schwartz, R and Owens, H 1968 Effects of isolation stress on female albino mice. Laboratory Animal Care 18: 426–435Google ScholarPubMed
Whimbey, AE and Denenberg, VH 1967 Two independent behavioral dimensions in open field performance. Journal of Comparative and Physiological Psychology 63: 500–504CrossRefGoogle ScholarPubMed
Wilmot, CA, VanderWende, C and Spoerlein, MT 1986 Behavioral and biochemical studies of dopamine receptor sensitivity in differentially housed mice. Psychopharmacology 89: 364–369CrossRefGoogle ScholarPubMed
Würbel, H, Freire, R and Nicol, CJ 1998a Prevention of stereo-typic wire-gnawing in laboratory mice: Effects on behaviour and implications for stereotypy as a coping response. Behavioral Processes 42: 61–72CrossRefGoogle Scholar
Würbel, H, Chapman, R and Rutland, C 1998b Effect of feed and environmental enrichment on development of stereotypic wire-gnawing in laboratory mice. Applied Animal Behaviour Science 60: 69–81CrossRefGoogle Scholar
Zimmermann, A, Stauffacher, M, Langhans, W and Würbel, H 2001 Enrichment dependent differences in novelty exploration in rats can be explained by habituation. Behavioural Brain Research 121: 11–20CrossRefGoogle ScholarPubMed