The open-field test is a commonly used apparatus in many behavioral studies. However, in most studies, temporal changes of details of behavior have been ignored. We thus examined open-field behavior as measured by both conventional indices and 12 ethograms supported by detailed temporal observation. To obtain a broader understanding, we used genetically diverse mouse strains: 10 wild-derived mouse strains (PGN2, BFM/2, HMI, CAST/Ei, NJL, BLG2, CHD, SWN, KJR, MSM), one strain derived from the so-called fancy mouse (JF1), and one standard laboratory strain, C57BL/6. Conventional measurements revealed a variety of relationships: some strains did not show the hypothesized association between high ambulation, longer stay in the central area, and low defecation. Our ethological approach revealed that some behaviors, such as freezing and jumping, were not observed in C57BL/6 but were seen in some wild-derived strains. Principal component analysis which included temporal information indicated that these strains had varied temporal patterns of habituation to novelty.
Similar content being viewed by others
References
Antoniou K., Kafetzopoulos E., (1991). A comparative study of the behavioral effects of d-amphetamine and apomorphine in the rat Pharmacol. Biochem. Biobehav. 39:61–70
Antoniou K., Kafetzopoulos E., Papadopoulou-Daifoti Z., Hyphantis T., Marselos M., (1998). d-Amphetamine, cocaine and caffeine: a comparative study of acute effects on locomotor activity and behavioural patterns in rats Neurosci. Biobehav. Rev. 23:189–196
Archer J., (1973). Tests for emotionality in rats and mice: a review Anim. Behav. 21:205–235
Bindra D., (1961). Components of general activity and the analysis of behavior Psychol. Rev. 68:205–215
Bindra D., Spinner N., (1958). Response to different degrees of novelty: the incidence of various activities J. Exp. Anal. Behav. 1:341–350
Blanchard D. C., Blanchard R. J., Rodgers R. J., (1991). Risk assessment and animal models of anxiety In Olivier B., Mos J., Slangen J. L., (eds), Animal models in psychopharmacology. Advances in pharmacological sciences Birkhauser Verlag Basel, Boston pp. 117–134
Blanchard R. J., Yudko E. B., Rodgers R. J., Blanchard D. C., (1993). Defense system psychopharmacology: an ethological approach to the pharmacology of fear and anxiety Behav. Brain Res. 58:155–165
Blizard D. A., (1971). Situational determinants of open-field behavior in Mus musculus Br. J. Psychol. 62:245–252
Bonhomme F., Guénet J.-L., (1996). The laboratory mouse and its wild relatives In Lyon M. F., Rastan S., Brown S. D. M., (eds), Genetic variants and strains of the laboratory mouse Oxford University Press Oxford, pp. 1577–1596
Broadhurst P. J., (1957). Determinants of emotionality in the rat: I. Situational factors Br. J. Psychol. 48:1–12
Broadhurst P. L., (1960). Experiments in psychogenetics: applications of biometrical genetics to the inheritance of behavior In Eysenck H. J., (eds), Experiments in personality: psychogenetics and psychopharmacology1 Routledge and Kegan Paul London pp. 1–102
Bruell J. H., (1969) Genetic and adaptive significance of emotional defecation in mice Ann. N.Y. Acad. Sci. 159:825–830
Carola V., D’Olimpio F., Brunamonti E., Mangia F., Renzi P., (2002). Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behavior in inbred mice Behav. Brain Res. 134:49–57
Choleris E., Thomas A. W., Kavaliers M., Prato F. S., (2001). A detailed ethological analysis of the mouse open field test: effects of diazepam, chlordiazepoxide, and an extremely low frequency pulsed magnetic field Neurosci. Biobehav. Rev. 25:235–260
Collins, R. L. (1966). What else does the defecation score measure? Proc. 74th Ann. Con. A. P. A., pp. 147–148
Crawley J. N., Belknap J. K., Collins A., Crabbe J. C., Frankel W., Henderson N., Hitzemann R. J., Maxson S. C., Miner L. L., Silva A. J., Wehner J. M., Wynshaw-Boris A., Paylor R., (1997). Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies Psychopharmacology 132:107–124
Crusio W. E., Schwegler H., van Ableen J. H. F., (1989). Behavioral responses to novelty and structural variation of the hippocampus in mice. I. Quantitative-genetic analysis of behavior in the open-field Behav. Brain Res. 32:75–80
DeFries J. C., Hegman J. P., (1970) Quantitative genetics and behavior: overview and perspective In Hirsch J., (eds), Behavior-genetic analysis McGraw-Hill New York pp. 322–339
Dudek B. C., Adams N., Boice R., Abbott M.E., (1983). Genetic influences on digging behaviors in mice (Mus musculus) in laboratory and seminatural settings J. Comp. Psychol. 97: 249–259
Dulawa S. C., Grandy D. K., Low M. J., Paulus M. P., Geyer M. A., (1999). Dopamine D4 receptor-knock-out mice exhibit reduced exploration of novel stimuli J. Neurosci. 19:9550–9556
Espejo E. F., (1997). Structure of the mouse behavior on the elevated plus-maze test of anxiety Behav. Brain Res. 86:105–112
Fernandes C., Liu L., Paya-Cano J. L., Gregorová S., Forejt J., Schalkwyk L. C., (2004). Behavioral characterization of wild derived male mice (Mus musculus musculus) of the PWD/Ph inbred strain: high exploration compared to C57BL/6J Behav. Genet. 34:621–629
Fernández-Teruel A., Escorihuela R. M., Gray J. A., Aguilar R., Gil L., Giménez-Llort L., Tobena A., Bhomra A., Nicod A., Mott R., Driscoll P., Dawson G. R., Flint J., (2002). A quantitative trait locus influencing anxiety in the laboratory rat Genome Res. 12:618–626
Flint J., Corley R., DeFries J. C., Fulker D. W., Gray J. A., Miller S., Collins A. C., (1995). A simple genetic basis for a complex psychological trait in laboratory mice Science 269:1432–1435
Furuse T., Blizard D. A., Moriwaki K., Miura Y., Yagasaki K., Shiroishi T., Koide T., (2002a). Genetic diversity underlying capsaicin intake in the Mishima battery of mouse strains Brain Res. Bull. 57:49–55
Furuse T., Takano-Shimizu T., Moriwaki K., Shiroishi T., Koide T., (2002b). QTL analyses of spontaneous activity by using mouse strains from Mishima battery Mamm. Genome 13:411–415
Furuse T., Miura Y., Yagasaki K., Shiroishi T., Koide T., (2003). Identification of QTLs for differential capsaicin sensitivity between mouse strains KJR and C57BL/6 Pain 105:169–175
Gallup G. G., Ledbetter D. H., Maser J. D., (1976) Strain differences among chickens in tonic immobility: evidence for an emotionality component J. Comp. Physiol. Psychol. 11:1075–1081
Gray J. A., (1965). A time-sample study of the components of general activity in selected strains of rats Can. J. Psychol. 19:74–82
Gershenfeld H. K., Neumann P. E., Mathis C., Crawley J. N., Li Z., Paul S. M., (1997). Mapping quantitative trait loci for open-field behavior in mice Behav. Genet. 27:201–210
Gershenfeld H. K., Paul S. M., (1997). Mapping quantitative trait loci for fear-like behaviors in mice Genomics 46:1–8
Hall C. S., (1934). Emotional behavior in the rat : I. Defecation and urination as measures of individual differences in emotionality J. Comp. Psychol. 18:385–403
Hall C. S., (1936). Emotional behavior in the rat : III. The relationship between emotionality and ambulatory activity J. Comp. Psychol. 22:345–352
Hall C. S., (1951). The genetics of behavior In Stevens S. S., (eds), Handbook of experimental psychology John Wiley & Sons Inc New York pp. 304–330
Holmes A., Parmigiani S., Ferrari P. F., Palanza P., Rodgers R. J., (2000). Behavioral profile of wild mice in the elevated plus-maze test for anxiety Physiol. Behav. 71:509–516
Koide T., Moriwaki K., Uchida L., Mita A., Sagai T., Yonekawa H., Katoh H., Miyashita N., Tsuchiya N., Nielsen T. J., Shiroishi T., (1998). A new inbred strain JF1 established from Japanese fancy mouse carrying the classic piebald allele Mamm. Genome 9:15–19
Koide T., Moriwaki K., Ikeda K., Niki H., Shiroishi T., (2000). Multi-phenotype behavioral characterization of inbred strains derived from wild stocks of Mus musculus Mamm. Genome 11:664–670
Logue S. F., Owen E. H., Rasmussen D. L., Wehner J. M., (1997). Assessment of locomotor activity, acoustic and tactile startle, and prepulse inhibition of startle in inbred mouse strains and F1 hybrids: implications of genetic background for single gene and quantitative trait loci analysis Neuroscience 80:1075–1086
Makino, J. (1983). Behavior genetic approach for the open-field behavior in the mouse. Ph.D. thesis, University of Tsukuba
Makino J., Kato K., Maes F. W., (1991). Temporal structure of open field behavior in inbred strains of mice Jpn. Psychol. Res. 33:145–152
Marks M. J., Miner L. L., Cole-Harding S., Burch J. B., Collins A. C., (1986). A genetic analysis of nicotine effects on open field activity Pharmacol. Biochem. Behav. 24:743–749
Moriwaki K., (1994)Wild mouse from a geneticist’s viewpoint In Moriwaki K., Shiroishi T., Yonekawa H., (eds), Genetics in wild mice Japan Sci. Soc. Press/S. Karger Tokyo/Baselpp. xiii–xxv
Ogasawara M., Imanishi T., Moriwaki K., Gaudieri S., Tsuda H., Hashimoto H., Shiroishi T., Gojobori T., Koide T., (2005) Length variation of CAG/CAA triplet repeats in 50 genes among 16 inbred mouse strains Gene 349:107–119
Pan R., Oxnard C., (2004) Craniodental variation in the African macaque, with reference to various Asian species Folia Primatol. 75: 355–375
Pardon M., Pérez-Diaz F., Joubert C., Cohen-Salmon C., (2000). Age-dependent effects of a chronic ultramild stress procedure on open-field behaviour in B6D2F1 female mice Physiol. Behav. 70:7–13
Ramos A., Correia E. C., Izídio G. S., Brüske G. R., (2003). Genetic selection of two new rat lines displaying different levels of anxiety-related behaviors Behav. Genet. 33:657–668
Ramos A., Moisan M.-P., Chaouloff F., Mormède C., Mormède P., (1999). Identification of female-specific QTLs affecting an emotionality-related behavior in rats Mol. Psychiatr. 4:453–462
Rodgers R. J., Johnson N. J. T., (1995). Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety Pharmacol. Biochem. Behav. 52:297–303
Royce J. R., (1977). On the construct validity of open-field measures Psychol. Bull. 84:1098–1106
Streng J., (1971). Open-field behavior in four inbred mouse strains Can. J. Psychol. 25:62–68
Suarez D. S., Gallup G. G., (1982) Open-field behavior in guinea pigs: developmental and adaptive considerations Behav. Proc. 7:267–274
Talbot C. J., Nicod A., Cherny S. S., Fulker D. W., Collins A. C., Flint J., (1999). High-resolution mapping of quantitative trait loci in outbred mice Nat. Genet. 21:305–308
Thompson W. R., (1953). The inheritance of behavior: behavioral differences in fifteen mouse strains Can. J. Psychol. 7:145–155
Treit D., Fundytus M., (1989). Thigmotaxis as a test for anxiolytic activity in rats Pharmacol. Biochem. Behav. 31:59–62
Trullas R., Skolnick P., (1993). Differences in fear motivated behaviors among inbred mouse strains Psychopharmacology 111:323–331
Turri M. G., Henderson N. D., DeFries J. C., Flint J., (2001a). Quantitative trait locus mapping in laboratory mice derived from a replicated selection experiment for open-field activity Genetics 158:1217–1226
Turri M. G., Datta S. R., DeFries J. C., Henderson N. D., Flint J., (2001b) QTL analysis identifies multiple behavioral dimensions in ethological tests of anxiety in laboratory mice Curr. Biol. 11:725–734
Vadasz C., Kobor G., Lajtha A., (1992). Motor activity and the mesotelencephalic dopamine function. I. High-resolution temporal and genetic analysis of open-field behavior Behav. Brain Res. 48:29–39
van Abeelen J. H. F., (1963). Mouse mutants studied by means of ethological methods: I. Ethogram Genetica 34:79–94
van Oortmerssen G. A., (1971) Biological significance, genetics and evolutionary origin of variability in behavior within and between inbred strains of mice (Mus musculus) Behavior 38:1–92
Walsh R. N., Cummins R. A., (1976). The open-field test: a critical review Psychol. Bull. 83:482–504
Acknowledgments
We are grateful to D. A. Blizard for comments on the manuscript, K. Moriwaki for his considerable work in establishing wild-derived strains, and to T. Takano for statistical advice. We thank all members of the Mouse Genomics Resource Laboratory at NIG for rearing the mice and for supporting this study. This study was supported by the Japan Society for the Promotion of Science, and by a Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology. This study is contribution number 2502 from the NIG.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Takahashi, A., Kato, K., Makino, J. et al. Multivariate Analysis of Temporal Descriptions of Open-field Behavior in Wild-derived Mouse Strains. Behav Genet 36, 763–774 (2006). https://doi.org/10.1007/s10519-005-9038-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10519-005-9038-3