Skip to main content
Log in

Paw preference and intra-/infrapyramidal mossy fibers in the hippocampus of the mouse

  • Published:
Behavior Genetics Aims and scope Submit manuscript

Abstract

The size of the intra-/infrapyramidal mossy fiber projections (IIP-MF) and their left/right asymmetry were assessed in 86 mice of either sex, including 26 animals from two mouse lines bred for strong or weak paw preference, 38 mice of a randomly bred F3 generation derived from an eight-way cross, and 22 mice with variably sized corpora callosa in which only the left hippocampus was measured. Prior to morphometry, all mice were tested for paw preference. In addition, we compared the strain means in paw preference as observed in nine inbred mouse strains with known differences in their IIP-MF distribution. Mice bred for strong paw preference had a 70% larger IIP-MF projection than weakly lateralized and dyscallosal mice; random-bred mice fell in-between the extremes. The individual scores of the strength of paw preference were positively correlated with the extent of the IIP-MF. Among the inbred strains, the extent of the IIP-MF was similarly correlated with the strength of paw preference. The acallosal mice showed a significant negative correlation between extent of the IIP-MF projection and test-retest reliability of paw use. The left-right asymmetry of the IIP-MF was significantly and positively correlated with the direction of paw preference in the entire sample. We conclude that size and asymmetry of the IIP-MF projection are some of the many factors influencing the direction of paw preference and its strength, albeit moderately. We hypothesize that mice with larger IIP-MF projections use a given paw more consistently, being perhaps more resistant to interferences, and that left-right asymmetries of the IIP-MF may bias and/or reinforce an initial choice of a paw. In addition, the data provide another example of correlations between IIP-MF variations and nonspatial behavior.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barber, R. P., Vaughn, J. E., Wimer, R. E., and Wimer, C. C. (1974). Genetically-associated variations in the distribution of dentate granule cell synapses upon the pyramidal cell dendrites in mouse hippocampus.J. Comp. Neurol. 156: 417–434.

    Article  PubMed  CAS  Google Scholar 

  • Barnéoud, P., and Van der Loos, H. (1993). Direction of handedness linked to hereditary asymmetry of a sensory system.Proc. Natl. Acad. Sci. USA 90: 3246–3250.

    PubMed  Google Scholar 

  • Barnéoud, P., Bronchti, G., and Van der Loos, H. (1994). Vision influences paw-preference in mice.Behav. Brain Res. 62: 157–164.

    PubMed  Google Scholar 

  • Bernasconi-Guastalla, S., Wolfer, D. P., and Lipp, H.-P. (1994). Hippocampal mossy fibers and swimming navigation in mice: Correlations with size and left-right asymmetries.Hippocampus 4: 53–64.

    Article  PubMed  CAS  Google Scholar 

  • Betancur, C., Neveu, P. J., and Le Moal, M. (1991). Strain and sex differences in the strength of paw preference in mice.Behav. Brain Res. 45: 97–101.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Büchel, C. (1993).Grössenvariationen des Corpus callosum bei Inzuchtmäusen und Hybriden und ihr Verhalten im Schwimmnavigationstest, M.D. thesis, Universität Zürich, Zürich.

    Google Scholar 

  • Cabib, S., D'Amato, F. R., Neveu, P. J., Deleplanque, B., Le Moal, M., and Puglisi-Allegra, S. (1995). Paw preference and brain dopamine asymmetries.Neuroscience 64: 427–432.

    Article  PubMed  CAS  Google Scholar 

  • Cassells, B., Collins, R. L., and Wahlsten, D. (1990). Path analysis of sex difference, forebrain commissure area and brain size in relation to degree of laterality in selectively bred mice.Brain. Res. 529: 50–56.

    Article  PubMed  CAS  Google Scholar 

  • Collins, R. L. (1979). Selective breeding for the degree of functional lateralization in mice.Behav. Genet. 9: 443–444.

    Google Scholar 

  • Collins, R. L. (1991). Reimpressed selective breeding for lateralization of handedness in mice.Brain Res. 564: 194–202.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Crusio, W. E. (1995). Natural selection on hippocampal circuitry underlying exploratory behaviour in mice: quantitative-genetic analysis. In Alleva, E., Fasolo, A., Lipp, H.-P., Nadel, L., and Ricceri, L. (eds.),Behavioural Brain Research in Naturalistic and Semi-Naturalistic Settings: Possibilities and Perspectives, Kluwer, Dordrecht, The Netherlands, pp. 323–342.

    Google Scholar 

  • Crusio, W. E., and Schwegler, H. (1987). Hippocampal mossy fiber distribution covaries with open-field habituation in the mouse.Behav. Brain Res. 26: 153–158.

    Article  PubMed  CAS  Google Scholar 

  • Crusio, W. E., Schwegler, H., and Lipp, H.-P., (1987). Radialmaze performance and structural variation of the hippocampus in mice: A correlation with mossy fibre distribution.Brain Res. 425: 182–185.

    Article  PubMed  CAS  Google Scholar 

  • Crusio, W. E., Schwegler, H., Brust, M., and van Abeelen, J. H. F. (1989a). Genetic selection for novelty-induced rearing behavior in mice produces changes in hippocampal mossy fiber distribution.J. Neurogenet. 5: 87–93.

    PubMed  CAS  Google Scholar 

  • Crusio, W. E., Schwegler, H., and van Abeelen, J. H. F. (1989b). Behavioral responses to novelty and structural variation of the hippocampus in mice. II. Multivariate genetic analysis.Behav. Brain Res. 32: 81–88.

    PubMed  CAS  Google Scholar 

  • Crusio, W. E., Bertholet, J.-Y., and Schwegler, H. (1990). No correlations between spatial and non-spatial reference memory in a T-maze task and hippocampal mossy fibre distribution in the mouse.Behav. Brain Res. 41 251–259.

    Article  PubMed  CAS  Google Scholar 

  • Crusio, W. E., Schwegler, H., and van Abeelen, J. H. F. (1991). Behavioural and neuroanatomical divergence between two sublines of C57BL/6J inbred mice.Behav. Brain Res. 42: 93–97.

    PubMed  CAS  Google Scholar 

  • Crusio, W. E., Schwegler, H., and Brust, I (1993). Covariations between hippocampal mossy fibres and working and reference memory in spatial and non-spatial radial maze tasks in mice.Eur. J. Neurosci. 5: 1413–1420.

    PubMed  CAS  Google Scholar 

  • Denenberg, V. H., Sherman G. F., Schrott, L. M., Rosen, G. D., and Galaburda, A. M. (1991). Spatial learning, discrimination learning, paw preference and neocortical ectopias in two autoimmune strains of mice.Brain Res. 562: 98–104.

    Article  PubMed  CAS  Google Scholar 

  • Gruber, D., Waanders, R., Collins, R. L., Wolfer, D. P., and Lipp, H.-P. (1991). Weak or missing paw preference in a muse strain (I/LnJ) with congenital absence of the corpus callosum.Behav. Brain Res. 45: 9–16.

    Google Scholar 

  • Guillot, P.-V., Roubertoux, P. L., and Crusio, W. E. (1994). Hippocampal mossy fiber distributions and intermale aggression in seven inbred mouse strains.Brain Res. 660: 167–169.

    Article  PubMed  CAS  Google Scholar 

  • Hausheer-Zarmakupi, Z., Wolfer, D. P., Leisinger-Trigona, M.-C., and Lipp, H.-P. (1996). Selective breeding for extremes in open-field activity of mice entails a differentiation of hippocampal mossy fibers.Behav. Genet. 26: 167–176.

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann, H. J., Wenkel, R., Schicknick, H., Bernstein, H.-G., and Schwegler, H. (1992). Hippocampal mossy fiber distribution does not correlate with two-way active avoidance performance in backcross lines derived from inbred mouse strains DBA/2 and C3H.Brain Res. 589: 171–174.

    Article  PubMed  CAS  Google Scholar 

  • Jamot, L., Bertholet, J.-Y., and Crusio, W. E. (1994). Neuroanatomical divergence between two substrains of C57BL/6J inbred mice entails differential radial-maze learning.Brain Res. 644: 352–356.

    Article  PubMed  CAS  Google Scholar 

  • Lipp, H.-P., and Schwegler, H. (1989). Structural variations of the hippocampal mossy fiber system and avoidance learning. In Köhler, C., and Chan-Palay, V. (eds.).The Hippocampus—New Vistas, Alan Liss, New York, pp. 295–307.

    Google Scholar 

  • Lipp, H.-P., and Wahlsten, D. (1992). Absence of the corpus callosum. In Driscoll, P. (ed.),Genetically-Defined Animal Models of Neuro-Behavioral Dysfunction, Birkhaeuser, Boston, pp. 217–252.

    Google Scholar 

  • Lipp, H.-P., and Wolfer, D. P. (1995). New paths towards old dreams: Microphrenology or the study of intact brains in intact worlds. In Alleva, E., Fasolo, A., Lipp, H.-P., Nadel, L., and Ricceri, L. (eds.).Behavioural Brain Research in Naturalistic and Semi-Naturalistic Settings: Possibilities and Perspectives, Kluwer, Dordrecht, The Netherlands, pp. 1–39.

    Google Scholar 

  • Lipp, H.-P., Collins, R. L., and Nauta, W. J. H. (1984). Structural asymmetries in brains of mice selected for strong lateralization.Brain Res. 310: 393–396.

    Article  PubMed  CAS  Google Scholar 

  • Lipp, H.-P., Schwegler, H., Crusio, W. E., Wolfer, D. P., Heimrich, B., Driscoll, P., and Leisinger-Trigona, M.-C. (1989). Using genetically-defined rodent strains for the identification of hippocampal traits relevant for two-way avoidance learning: A non-invasive approach.Experientia 45: 845–859.

    Article  PubMed  CAS  Google Scholar 

  • McManus, I. C. (1992). Are paw preference differences in HI and LO mice the result of specific genes or of heterosis and fluctuating asymmetry?Behav. Genet. 22: 435–451.

    Article  PubMed  CAS  Google Scholar 

  • Nadel, L. (1995). The psychobiology of spatial behavior: The hippocampal formation and spatial mapping. In Alleva, E., Fasolo, A., Lipp, H.-P., Nadel, L., and Ricceri, L. (eds.),Behavioural Brain Research in Naturalistic and Semi-Naturalistic Settings: Possibilities and Perspectives, Kluwer, Dordrecht, The Netherlands, pp. 245–258.

    Google Scholar 

  • Neveu, P. J., Barnéoud, P., Vitiello, S., Betancur, C., and Le Moal, M. (1988). Brain modulation of the immune system: Association between lymphocyte responsiveness and paw preference in mice.Brain Res. 457: 392–394.

    Article  PubMed  CAS  Google Scholar 

  • Neveu, P. J., Betancur, C., Vitiello, S., and Le Moal, M. (1991). Sex-dependent association between immune function and paw preference in two substrains of C3H mice.Brain Res. 559: 347–351.

    Article  PubMed  CAS  Google Scholar 

  • Nosten, M., Roubertoux, P., Degrelle, H., and Leboyer, M. (1989). Effect of the Tfm mutation on handedness in mice.J. Endocrinol. 121: R5-R7.

    PubMed  CAS  Google Scholar 

  • O'Keefe, J., and Nadel, L. (1978).The Hippocampus as a Cognitive Map, Clarendon Press, Oxford.

    Google Scholar 

  • Roderick, T. H., Wimer, R. E., and Wimer, C. C. (1976). Genetic manipulation of neuroanatomical traits. In Petrinovich, L., and McGaugh, J. L. (eds.),Knowing, Thinking, and Believing, Plenum Press, New York, pp. 143–178.

    Google Scholar 

  • Roullet, P., and Lassalle, J. M. (1992). Behavioural strategies, sensorial processes and hippocampal mossy fibre distribution in radial maze performance in mice.Behav. Brain Res. 48: 77–85.

    PubMed  CAS  Google Scholar 

  • Schöpke, R., Wolfer, D. P., Lipp, H.-P., and Leisinger-Trigona, M.-C. (1991). Swimming navigation and structural variations of the infrapyramidal mossy fibers in the hippocampus of the mouse.Hippocampus 1: 315–328.

    Article  PubMed  Google Scholar 

  • Schwegler, H., and Crusio, W. E. (1995). Correlations between radial-maze learning and structural variations of septum and hippocampus in rodents.Behav. Brain Res. 67: 29–41.

    Article  PubMed  CAS  Google Scholar 

  • Schwegler, H., and Lipp, H.-P. (1983). Hereditary covariations of neuronal circuitry and behavior: Correlations between the proportions of hippocampal synaptic fields in the regio inferior and two-way avoidance in mice and rats.Behav. Brain Res. 7: 1–39.

    Article  PubMed  CAS  Google Scholar 

  • Schwegler, H., and Lipp, H.-P. (1995). Variations in the morphology of the septohippocampal complex and maze learning in rodents: Correlation between morphology and behavior. In Alleva, E., Fasolo, A., Lipp, H.-P., Nadel, L., and Ricceri, L. (eds.).Behavioural Brain Research in Naturalistic and Semi-Naturalistic Settings: Possibilities and Perspectives, Kluwer, Dordrecht, The Netherlands, pp. 259–276.

    Google Scholar 

  • Schwegler, H., Crusio, W. E., and Brust, I. (1990). Hippocampal mossy fibers and radial-maze learning in the mouse: A correlation with spatial working memory but not with non-spatial reference memory.Neuroscience 34: 293–298.

    Article  PubMed  CAS  Google Scholar 

  • Schwegler, H., Mueller, G. G., Crusio, W. E., Szemes, L., and Seress, L. (1993). Hippocampal morphology and spatially related behavior in Long-Evans and CFY rats.Hippocampus,3: 1–8.

    Article  PubMed  CAS  Google Scholar 

  • Signore, P., Chaoui, M., Nosten-Bertrand, M., Perez Diaz, F., and Marchaland, C. (1991a). Handedness in mice: Comparison across eleven inbred strains.Behav. Genet. 21: 421–429.

    Article  PubMed  CAS  Google Scholar 

  • Signore, P., Nosten-Bertrand, M., Chaoui, M., Roubertoux, P. L., Marchaland, C., and Perez Diaz, F. (1991b). An assessment of handedness in mice.Physiol. Behav. 49: 701–704.

    Article  PubMed  CAS  Google Scholar 

  • Sluyter, F., Jamot, L., Van Oortmerssen, G. A., and Crusio, W. E. (1994). Hippocampal mossy fiber distributions in mice selected for aggression.Brain Res. 646: 145–148.

    Article  PubMed  CAS  Google Scholar 

  • Takeda, S., and Endo, A. (1993). Paw preference in mice: A reappraisal.Physiol. Behav. 53: 727–730.

    Article  PubMed  CAS  Google Scholar 

  • Wahlsten, D., Lassalle, J.-M., and Bulman-Fleming, B. (1991). Hybrid vigour and maternal environment in mice. III. Hippocampal mossy fibres and behaviour.Behav. Process. 23: 47–57.

    Google Scholar 

  • Ward, R., Tremblay, L., and Lassonde, M. C. (1987). The relationship between callosal variation and lateralization in mice is genotype-dependent.Brain Res. 424: 84–88.

    Article  PubMed  CAS  Google Scholar 

  • Waters, N. S., and Denenberg, V. H. (1991). A measure of lateral paw preference in the mouse.Physiol. Behav. 50: 853–856.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hans-Peter Lipp.

Additional information

We are deeply saddened by her untimely death.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lipp, HP., Collins, R.L., Hausheer-Zarmakupi, Z. et al. Paw preference and intra-/infrapyramidal mossy fibers in the hippocampus of the mouse. Behav Genet 26, 379–390 (1996). https://doi.org/10.1007/BF02359482

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02359482

Key words

Navigation