Abstract
Lateralization of paw usage in the laboratory mouse may be a useful model system in which to assess the genetic and developmental cause of asymmetry of hand usage. With a set number of paw reaches from a centrally placed food tube, individual mice from an inbred strain will exhibit a reliable number of left and right paw reaches. For a single inbred strain, there are approximately equal numbers of left-pawed and right-pawed mice, but strain differences have been reported in the degree of lateralization of paw preference. We reported a preliminary strain survey in which the strains appeared to fall into two groups of highly lateralized and weakly lateralized paw preference (Biddleet al., 1993). We review here our expanded survey of genetically different strains and stocks of the laboratory mouse, including different species and subspecies. The major genetic trait is the degree of lateralization of paw preference and the strain differences appear to fall into three major classes of highly lateralized, weakly lateralized, and ambilateral preference. The trait exhibits both additivity and dominance in preliminary reciprocal crosses, depending on which strain pairs are used. The wide difference between strains that have highly lateralized and ambilateral paw preference suggests specific genetic tools that could be used to begin a genetic dissection of the causes of this trait. Preliminary assessment of the size of the corpus callosum in three strains with significantly different degrees of lateralization suggests that genetically determined deficiencies and absence of this structure are not the direct cause of the strain differences in the trait of degree of lateralization. In the expanded survey, some strains appear to exhibit a directional deviation from equal numbers of mice with left and right paw usage. Therefore, direction of paw usage may not be a genetically neutral trait, but replicate assessments and genetic tests are needed to confirm this.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bailey, D. W. (1981). Recombinant inbred strains and bilineal congenic strains. In Foster, H. L., Small, J. D., and Fox, J. G. (eds.),The Mouse in Biomedical Research, Vol. I. History, Genetics, and Wild Mice, Academic Press New York, pp. 223–239.
Beermann, F., Ruppert, S., Hummler, E., and Schutz, G. (1991). Tyrosinase as a marker for transgenic mice.Nucl. Acids. Res. 19: 958.
Biddle, F. G., and Eales, B. A. (1991). Strain variation in venous heterotaxias in the mouse.Teratology 43: 432.
Biddle, F. G., and Fraser, F. C. (1979). Genetic independence of the embryonic reactivity difference to cortisone-and 6-aminonicotinamide-induced cleft palate in the mouse.Teratology 19: 207–212.
Biddle, F. G., and Fraser, F. C., (1986). Major gene determination of liability to spontaneous cleft lip in the mouse.J. Craniofac. Genet. Dev. Biol. Suppl. 2: 67–88.
Biddle, F. G., and Nishioka, Y. (1988). Assays of testis development in the mouse distinguish three classes ofdomesticus-type Y chromosome.Genome 30: 870–878.
Biddle, F. G., Jung, J. D., and Eales, B. A. (1991). Genetically determined variation in the azygos vein in the mouse.Teratology 44: 675–683.
Biddle, F. G., Coffaro, C. M., Ziehr, J. E., and Eales, B. A. (1993). Genetic variation in paw preference (handedness) in the mouse.Genome 36: 935–943.
Bock, G. R., and Marsh, J. (eds.) (1991).Biological Asymmetry and Handedness, Ciba Foundation Symposium 162, Wiley-Interscience, Chichester.
Brueckner, M., D'Eustachio, P. D., and Horwich, A. L. (1989). Linkage mapping of a mouse gene,iv, that controls leftright asymmetry of the heart and viscera.Proc. Natl. Acad. Sci. USA 86: 5035–5038.
Collins, R. L. (1968). On the inheritance of handedness. I. Laterality in inbred mice.J. Hered. 59: 9–12.
Collins, R. L. (1969). On the inheritance of handedness. II. Selection for sinistrality in mice.J. Hered. 60: 117–119.
Collins, R. L. (1985). On the inheritance of direction and degree of asymmetry. In Glick, S. D. (ed.),Cerebral Lateralization in Non-human Species, Academic Press, New York, pp. 41–71.
Collins, R. L., Sargent E. E., and Neumann, P. E. (1993). Genetic and behavioral tests of the McManus hypothesis relating response to selection for lateralization of handedness in mice to degree of heterozygosity.Behav. Genet. 23:413–421.
Copeland, N. G., Jenkins, N. A., Gilbert, D. J., Eppig, J. T., Maltais, L. J., Miller, J. C., Dietrich, W. F., Weaver, A., Lincoln, S. E., Steen, R. G., Stein, L. D., Nadeau, J. H., and Lander, E. S. (1993). A current linkage map of the mouse: Current applications and future prospects.Science 262: 57–66.
Cunliffe-Beamer, T. L. (1983). Biomethodology and surgical techniques. In Foster, H. L., Small, J. D., and Fox, J. G. (eds.),The Mouse in Biomedical Research, Vol. III. Normative Biology, Immunology and Husbandry, Academic Press, New York, pp. 401–437.
Dietrich, W., Katz, H., Lincoln, S. E., Shin, H.-S., Friedman, J., Dracopoli, N. C., and Lander, E. S. (1992). A genetic map of the mouse suitable for typing intraspecific crosses.Genetics 131: 423–447.
Dietrich, W. F., Miller, J. C., Steen, R. G., Merchant, M., Damron, D., Nahlf, R., Gross, A., Joyce, D.C., Wessel, M., Dredge, R. D., Marquis, A., Stein, L. D., Goodman, N., Page, D. C., and Lander, E. S. (1994). A genetic map of the mouse with 4,006 simple sequence length polymorphisms.Nature Genet. 7: 220–245.
Elston, R. C., and Stewart, J. (1970). A new test of association of continuous variables.Biometrics 26: 305–314, and 860.
Festing, M. F. W. (1979).Inbred Strains in Biomedical Research, Oxford University Press, New York.
Festing, M. F. W. (1992). From character to gene: Some strategies for identifying single genes controlling behavioral characters In Goldowitz, D., Wahlsten, D., and Wimer, R. E. (eds.),Techniques for the Genetic Analysis of Brain and Behavior: Focus on the Mouse, Elsevier Science, Amsterdam, pp. 17–38.
Green, M. C. (1967). A defect in the splanchnic, mesoderm caused by the mutant gene dominant hemimelia in the mouse.Dev. Biol. 15: 62–89.
Gruber, D., Waanders, R., Collins, R. L., Wolfer, D. P., and Lipp, H.-P. (1991). Weak or missing paw lateralization in a mouse strain (I/LnJ) with congenital absence of the corpus callosum.Behav. Brain Res. 46: 9–16.
Layton, W. M. (1976). Random determination of a developmental process: Reversal of normal visceral asymmetry in the mouse.J. Hered 67: 336–338.
Lipp, H.-P., and Wahlsten, D. (1992). Absence of the corpus callosum. In Driscoll, P. (ed.),Genetically Defined Animal Models of Neurobehavioral Dysfunctions, Birkhauser, Boston, pp. 217–252.
Livy, D. J., and Wahlsten, D. (1991). Tests of genetic allelism between four inbred mouse strains with absent corpus callosum.J. Hered. 82:459–464.
Lyon, M. F., and Searle, A. G. (1989).Genetic Variants and Strains of the Laboratory Mouse, 2nd ed., Oxford University Press, Oxford.
Morishima, M., Ando, M., and Takao, A. (1991). visceroatrial heterotaxy syndrome in the NOD mouse with special reference to atrial situs.Teratology 44: 91–100.
Potter, M. (1986). Listing of stocks and strains of mice in the genusMus derived from the feral state.Curr. Topics Microbiol. Immunol. 127: 373–395.
Schmued, L. C. (1990). A rapid, sensitive histochemical stain for myelin in frozen brain sections.J. Histochem. Cytochem. 38: 717–720.
Siegel, S., (1956).Nonparametric Statistics for the Behavioral Sciences, McGraw-Hill, New York.
Sokal, R. R., and Rohlf, F. J. (1969),Biometry. The Principles and Practice of Statistics in Biological Research, W. H. Freeman, San Francisco.
Stewart, J. (1969). Biometrical genetics with one or two loci. I. The choice of a specific genetic model.Heredity 24: 211–224.
Stewart, J., and Elston, R. C. (1973). Biometrical genetics with one or two loci: The inheritance of physiological characters in mice.Genetics 73: 675–693.
Taylor, B. A. (1972). Genetic relationships between strains of mice.J. Hered. 63: 83–86.
Tukey, J. W. (1977)Exploratory Data Analysis, Addison-Wesley, Reading, MA.
Wahlsten, D. (1982). Mode of inheritance of deficient corpus callosum in mice.J. Hered. 73: 281–285.
Waters, N. S., and Denenberg, V. H. (1991). A measure of lateral paw preference in the mouse.Physiol. Behav. 50: 853–856.
Waters, N. S., and Denenberg, V. H. (1994). Analysis of two measures of paw preference in a large population of inbred mice.Behav. Brain Res. 63: 195–204.
Yokoyama, T., Copeland, N. G., Jenkins, N. A., Montgomery, C. A., Elder, F. F. B., and Overbeek, P. A. (1993). Reversal of left-right asymmetry: A situs inversus mutation.Science 260: 679–682.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Biddle, F.G., Eales, B.A. The degree of lateralization of paw usage (handedness) in the mouse is defined by three major phenotypes. Behav Genet 26, 391–406 (1996). https://doi.org/10.1007/BF02359483
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02359483