Summary
Genetically-defined rodent strains permit the identification of hippocampal traits which are of functional relevance for the performance of two-way avoidance behavior. This is exemplified here by analyzing the relationship between infrapyramidal mossy fibers (a tiny projection terminating upon the basal dendrites of hippocampal pyramidal neurons) and two-way avoidance learning in about 800 animals. The necessary steps include 1) identification of structural traits sensitive to selective breeding for extremes in two-way avoidance, 2) testing the robustness of the associations found by studying individual and genetical correlations between hippocampal traits and behavior, 3) establishing causal relationships by Mendelian crossing of strains with extreme structural traits and studying the behavioral consequences of such structural ‘randomization’, 4) confirming causal relationships by manipulating the structural variable in inbred (isogenic) strains, thereby eliminating the possibility of genetic linkage, and 5) ruling out the possibility of spurious associations by studying the correlations between the hippocampal trait and other behaviors known to depend on hippocampal functioning.
In comparison with the classical lesion approach for identifying relationships between brain and behavior, the present procedure appears to be superior in two aspects: it is non-invasive, and it focuses automatically on those brain traits which are used by natural selection to shape behaviorally-defined animal populations, i.e., it reveals the natural regulators of behavior.
Similar content being viewed by others
Literatur
Altman, J., and Das, G. D., Postnatal neurogenesis in the guinea pig. Nature214 (1967) 1098–1101.
Amaral, D. G., A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. comp. Neurol.182 (1978) 851–914.
Amaral, D. G., and Dent, J. A., Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J. comp. Neurol.195 (1981) 51–86.
Barber, R. P., Vaughn, J. E., Wimer, R. E., and Wimer, C. C., Genetically-associated variations in the distribution of dentate granule cell synapses upon the pyramidal cell dendrites in mouse hippocampus. J. comp. Neurol.156 (1974) 417–434.
Bayer, S. A., Yacke, S. W., and Puri, P. S., Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science216 (1982) 890–892.
Bignami, G., and Bovet, D., Experience de sélection par rapport à une réaction conditionnée d'évitement chez le rat. C. r. Acad. Sci. (Paris)260 (1965) 1239–1244.
Bignami, G., and Michalek, H., Cholinergic mechanisms and aversively motivated behavior, in: The Psychopharmacology of Aversively Motivated Behavior, pp. 173–255. Eds H. Anisman and G. Bignami. Plenum Press, New York 1978.
Bovet, D., Bovet-Nitti, F., and Oliverio, A., Genetic aspects of memory and learning in mice. Science163 (1969) 139–149.
Broadhurst, P. L., Experiments in psychogenetics: applications of biometrical genetics for the inheritance of behavior, in: Experiments in Personality, vol. 1, Psychogenetics and Psychopharmacology, pp. 1–102. Ed. H. J. Eysenck. Routledge and Kegan, London 1960.
Buselmaier, W., Vierling, T., Balzereit, W., and Schwegler, H., Genetic analysis of avoidance learning by means of different psychological testing systems with inbred mice as model organisms. Psychol. Res.43 (1981) 317–333.
Cassell, M. D., and Brown, M. W., The distribution of Timm's stain in the nonsulphide-perfused human hippocampal formation. J. comp. Neurol.222 (1984) 461–471.
Coleman, P. D., Flood, D. G., and West, M. J., Volumes of the components of the hippocampus in the aging F344 rat. J. comp. Neurol.266 (1987) 300–306.
Collins, R. L., Inheritance of avoidance conditioning in mice: a diallel study. Science143 (1964) 1188–1190.
Collins, R. L., Selective breeding for the degree of functional lateralization in mice. Behav. Genet.9 (1979) 443–444.
Collins, R. L., On the inheritance of direction and degree of asymmetry, in: Cerebral Lateralization in Nonhuman Species, pp. 41–71. Ed. S. D. Glick, Academic Press, New York 1985.
Cook, T. M., and Crutcher, K. A., Extensive target cell loss during development results in mossy fibers in the regio superior (CA1) of the rat hippocampal formation. Brain Res.353 (1985) 19–30.
Cooper, S. J., and Webb, Z. M., Microstructural analysis of chlordiazepoxide's effects on food preference behavior in roman high-, control- and low-avoidance rats. Physiol. Behav.32 (1984) 581–588.
Crusio, W. E., Genthner-Grimm, G., and Schwegler, H., A quantitative-genetic analysis of hippocampal variation in the mouse. J. Neurogenet.3 (1986) 203–214.
Crusio, W. E., and Schwegler, H., Hippocampal mossy fiber distribution covaries with open-field habituation in the mouse. Behav. Brain Res.26 (1987) 153–158.
Crusio, W. E., Schwegler, H., Brust, M., and Van Abeelen, J. H. F., Genetic selection for novelty-induced rearing behavior in mice produces changes in hippocampal mossy fiber distribution. J. Neurogenet.5 (1989) 87–93.
Crusio, W. E., Schwegler, H., and Lipp, H.-P., Radial-maze performance and structural variation of the hippocampus in mice: a correlation with mossy fibre distribution. Brain Res.425 (1987) 182–185.
D'Angio, M., Serrano, A., Driscoll, P., and Scatton, B., Stressful environmental stimuli increase extracellular DOPAC-3 levels in the prefrontal cortex of hypoemotional (Roman High Avoidance) but not hyperemotional (Roman Low Avoidance) rats. An in vivo voltammetric study. Brain Res.451 (1988) 237–247.
Danscher, G., Histochemical demonstration of heavy metals. Histochemistry70 (1981) 1–16.
DeFries, J. C., Gervais, M. C., and Thomas, E. A., Response to 30 generations of selection for open-field activity in laboratory mice. Behav. Genet.8 (1978) 3–13.
Delacour, J., Coulon, J. F., David, J. C., and Guénaire, C., Brain octopamine and strain differences in avoidance behavior. Brain Res.288 (1983) 169–176.
Dimitrieva, N. I., Gozzo, S., Dimitriev, Y., and Ammassari-Teule, M., Mossy fiber distribution in four lines of rats: a correlative study with avoidance abilities and excitability thresholds. Physiol. Psychol.12 (1984) 30–34.
Driscoll, P., Roman high- and low-avoidance rats: present status of the Swiss sublines, RHA/Verh and RLA/Verh, and effects of amphetamine on shuttle-box performance. Behav. Genet.16 (1986) 355–364.
Driscoll, P., and Baettig, K., Behavioral, emotional and neurochemical profiles of rats selected for extreme differences in active, two-way avoidance performance, in: Genetics of the Brain, pp. 95–123. Ed. I. Lieblich. Elsevier, Amsterdam 1982.
Dudek, B. C., and Abbott, M. C., A biometrical genetic analysis of ethanol response in selectively bred long-sleep and short-sleep mice. Behav. Genet.14 (1984) 1–20.
Eckenhoff, M. F., and Rakic, P., Nature and fate of proliferative cells in the hippocampal dentate gyrus during the lifespan of the Rhesus monkey. J. Neurosci.8 (1988) 2729–2747.
Edwards, A. L., Multiple Regression and the Analysis of Variance and Covariance. W. H. Freeman, San Francisco 1979.
Elkins, R. L., Separation of taste-aversion-prone and taste-aversion-resistant rats through selective breeding: implications for individual differences in conditionability and aversion-therapy alcoholism treatment. Behav. Neurosci.100 (1986) 121–124.
Flechsig, P., Die Leitungsbahnen im Gehirn und Rückenmark des Menschen auf Grund entwicklungsgeschichtlicher Untersuchungen. Wilhelm Engelmann, Leipzig 1876.
Flechsig, P., Anatomie des menschlichen Gehirns und Rückenmarks auf myelogenetischer Grundlage. Georg Thieme, Leipzig 1920.
Flühmann, S., Lipp, H.-P., and Schwegler, H., A possible role of infrapyramidal mossy fiber terminals in aversively motivated decision making of mice in a Y-maze. Neuosci. Lett. Suppl.7 (1981) S237.
Frotscher, M., and Zimmer, J., Lesion-induced mossy fibers to the molecular layer of the rat fascia dentata: identification of postsynaptic granule cells by the Golgi-EM technique. J. comp. Neurol.215 (1983) 299–311.
Fuller, J. L., and Thompson, W. R., Foundations of Behavior Genetics. C. V. Mosby, St. Louis 1978.
Gall, F. J., Sur les Fonctions du Cerveau et sur Celles de chacune de ses Parties, vol. 1–6. Baillière, Paris 1822.
Gall, F. J., Franz Josef Gall, Naturforscher und Anthropologe; Ausgewählte Texte. Ed. E. Lesky. Hans Huber, Bern 1979.
Gentsch, C., Lichsteiner, M., and Feer, H., 3H-diazepam binding sites in Roman high- and Roman low-avoidance rats. Experientia37 (1981) 1315–1316.
Gentsch, C., Lichtsteiner, M., and Feer, H., Regional distribution of 3H-imipramine-binding sites in the CNS of Roman high and low avoidance rats. Eur. J. Pharmac.88 (1983) 259–261.
Gozzo, S., and Ammassari-Teule, M., Different mossy fiber patterns in two inbred strains of mice: a functional hypothesis. Neurosci. Lett.36 (1983) 111–116.
Guénaire, C., and Delacour, J., Differential acquisition of a ‘working memory’ task by the Roman strains of rats. Physiol. Behav.34 (1985) 705–707.
Hall, R. D., and Macrides, F., Olfactory bulbectomy impairs the rat's radial-maze behavior. Physiol. Behav.30 (1983) 797–803.
Harley, C. W., Arm choices in a sunburst maze: effects of hippocampectomy in the rat. Physiol. Behav.23 (1979) 283–290.
Haug, F. M. S., Electron microscopical localization of the zinc in the hippocampal mossy fibre synapses by a modified sulfide silver procedure. Histochemie8 (1967) 355–368.
Haug, F. M. S., Heavy metals in the brain. A light microscopic study of the rat with Timm's sulphide silver method. Methodological considerations and cytological and regional staining patterns. Adv. Anat. Embryol. Cell. Biol.47 (1973) 1–71.
Haug, F. M. S., Light microscopical mapping of the hippocampal region, the pyriform cortex, and the cortico-medial amygdaloid nuclei of the rat with Timm's sulphide silver method. I. Area dentata, hippocampus and subiculum. Z. Anat. Entw. Gesch.145 (1974) 1–27.
Hausheer-Zarmakupi, Z., Lipp, H.-P., Wolfer, D. P., and Leisinger-Trigona, M.-C., Selective breeding for a non-spatial behavior of mice entails a morphological differentiation of the hippocampal mossy fibers. Eur. J. Neurosci. Suppl.1 (1988) 252.
Hegmann, J. P., and Possidente, B., Estimating genetic correlations from inbred strains. Behav. Genet.11 (1981) 103–114.
Heimrich, B., Schwegler, H., and Crusio, W. E., Hippocampal variation between the inbred mouse strains C3H/HeJ and DBA/2: a quantitative-genetic analysis. J. Neurogenet.2 (1985) 389–401.
Heimrich, B., Schwegler, H., Crusio, W. E., and Buselmaier, W., Substrain divergence in C3H inbred mice. Behav. Genet.18 (1988) 671–674.
Hyde, J. S., and Sawyer, T. F., Selection for agonistic behavior in wild female mice. Behav. Genet.10 (1980) 349–359.
Katz, M. J., and Lasek, R. J., Evolution of the nervous system: role of ontogenetic mechanisms in the evolution of matching populations. Proc. natl Acad. Sci. USA75 (1978) 1349–1352.
Katz, M. J., Lasek, R. J., and Kaiserman-Abramof, I. R., Ontophyletics of the nervous system: eyeless mutants illustrate how ontogenetic buffer mechanisms channel evolution. Proc. natl Acad. Sci. USA78 (1981) 397–401.
Kolb, B., and Nonneman, A. J., Functional development in prefrontal cortex continues into adolescence. Science193 (1976) 33–36.
Lagerspetz, K. Y. H., Tirri, R., and Lagerspetz, K. M. J., Neurochemical and endocrinological studies of mice selectively bred for aggressiveness. Scand. J. Psychol.9 (1968) 157–160.
Lauder, J. M., and Mugnaini, E., Early hyperthyroidism alters the distribution of mossy fibres in the rat hippocampus. Nature268 (1977) 335–337.
Laurberg, S., and Zimmer, J., Lesion-induced rerouting of hippocampal mossy fibers in developing but not in adult rats. J. comp. Neurol.190 (1980) 627–650.
Leiner, H. C., Leiner, A. L., and Dow, R. S., Does the cerebellum contribute to mental skills? Behav. Neurosci.100 (1986) 443–454.
Lieblich, I., Cohen, E., and Beiles, A., Selection for high and for low rates of self-stimulation in rats. Physiol. Behav.21 (1978) 843–849.
Lieblich, I., Driscoll, P., and Lipp, H.-P., Genetic relation between the readiness to self-stimulate lateral hypothalamus, two-way avoidance learning and the proportions of hippocampal synaptic fields in region inferior. Behav. Genet.17 (1987) 427–438.
Lipp, H.-P., Brain complexity enhances speed of behavioral evolution. Behav. Brain Sci.2 (1979) 42.
Lipp, H.-P., Differential hypothalamic self-stimulation behaviour in Roman high-avoidance and low-avoidance rats. Brain Res. Bull.4 (1979) 553–559.
Lipp, H.-P., Postnatal development of hippocampal mossy fiber circuitry and freezing behavior in the guinea-pig. Neurosci. Lett. Suppl.22 (1985) S332.
Lipp, H.-P., The forebrain as a playground of mammalian evolution, in: Intelligence and Evolutionary Biology. NATO ASI Series Vol. G 17, pp. 109–118. Eds. H. J. Jerison and I. Jerison. Springer, Berlin/Heidelberg 1988.
Lipp, H.-P., Is the hippocampus a cerebellum of the limbic system?, Verh. Anat. Ges. (1989) in press.
Lipp, H.-P., Leisinger-Trigona, M.-C., and Schwegler, H., Selective breeding for differential open-field activity of mice entails a differentiation of hippocampal mossy fibers. Neurosci. Lett. Suppl.26 (1986) S109.
Lipp, H.-P., and Schwegler, H., Hippocampal mossy fibers and avoidance learning, in: Genetics of the Brain, pp. 325–364. Ed. I. Lieblich. Elsevier, Amsterdam 1982.
Lipp, H.-P., and Schwegler, H., Structural variations of the hippocampal mossy fiber system and avoidance learning, in: The Hippocampus-New Vistas, pp. 295–307. Eds C. Köhler and V. Chan-Palay. Alan Liss Inc. New York 1989.
Lipp, H.-P., Schwegler, H., and Driscoll, P., Postnatal modification of hippocampal circuitry alters avoidance learning in adult rats. Science225 (1984) 80–82.
Lipp, H.-P., Schwegler, H., and Hausheer-Zarmakupi, Z., The infrapyramidal mossy fiber projection in the hippocampus of the mouse: a positive correlation with Y-maze avoidance learning. Soc. Neurosci. Abstr.12 (1986) 751.
Lipp, H.-P., Schwegler, H., Heimrich, B., Cerbone, A., and Sadile, A. G., Strain-specific correlations between hippocampal structural traits and habituation in a spatial novelty situation. Behav. Brain Res.24 (1987) 111–123.
Lipp, H.-P., Schwegler, H., Heimrich, B., and Driscoll, P., Infrapyramidal mossy fibers and two-way avoidance learning: developmental modification of hippocampal circuitry and adult behavior of rats and mice. J. Neurosci.8 (1988) 1905–1921.
Lipp, H.-P., Schöpke, R., Wolfer, D.P., Schwegler, H., and Leisinger-Trigona, M.-C., Hippocampal mossy fiber variations and swimming navigation in mice. Behav. Brain Res. (1989) in print.
Lynch, C. B., Response to divergent selection for nesting behavior inMus musculus. Genetics96 (1980) 757–767.
Mair, R. G., Gellman, R. L., and Gesteland, R. C., Postnatal proliferation and maturation of olfactory bulb neurons in the rat. Neurosci.7 (1982) 3105–3116.
McClearn, G. E., The genetics of mouse behavior in novel situations. J. comp. physiol. Psychol.52 (1959) 62–67.
Messeri, P., Oliverio, A., and Bovet, D., Relations between avoidance and activity: a diallel study in mice. Behav. Biol.7 (1972) 733–742.
Morris, R. G. M., Development of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Meth.11 (1984) 47–60.
Morris, R. G. M., Garrud, P., Rawlins, J. N. P., and O'Keefe, J., Place navigation impaired in rats with hippocampal lesions. Nature297 (1982) 681–683.
Morse, H. C. III, Historical perspective on the development of inbred mice, in: Origins of Inbred Mice. Ed. H. C. Morse III. Academic Press, New York 1979.
Nadler, J. V., Perry, B. W., Gentry, C., and Cotman, C. W., Fate of the hippocampal mossy fiber projection after destruction of its post-synaptic targets with intraventricular kainic acid. J. comp. Neurol.196 (1981) 549–569.
Nagy, Z. M., and Misanin, J. R., Visula perception in the retinal degenerate C3H mouse. J. comp. physiol. Psychol.72 (1970) 306–310.
Nesbitt, M. N., Spence, M. A., and Butler, K., Behavior in chimeric mice combining differently behaving strains. Behav. Genet.9 (1979) 277–287.
Nowakowski, R. S., The mode of inheritance of a defect in lamination in the hippocampus of BALB/c mice. J. Neurogenet.1 (1984) 249–258.
O'Keefe, J., and Nadel, L., The Hippocampus as a Cognitive Map. Clarendon Press, Oxford 1978.
Oliverio, A., and Castellano, C., Postnatal brain maturation and learning in the mouse. In: Genetics, Environment and Intelligence, pp. 118–131. Ed. A. Oliverio. Elsevier, Amsterdam 1977.
Oliverio, A., Eleftheriou, B. E., and Puglisi-Allegra, S., A genetic approach to behavioral plasticity and rigidity, in: Theoretical Advances in Behavior Genetics, pp. 139–168. Eds J. R. Royce and L. P. Mos. Sijthoff and Noordhoff, Alphen-Germantown 1979.
Oliverio, A., and Messeri, P., An analysis of single gene effects on avoidance, maze, wheel-running and exploratory behavior in the mouse. Behav. Biol.8 (1973) 771–783.
Olton, D. S., Becker, J. T., and Handelmann, G. E., Hippocampus, space, and memory. Behav. Brain Sci.2 (1979) 313–365.
Olton, D. S., and Werz, M. A., Hippocampal function and behavior: Spatial discrimination and response inhibition. Physiol. Behav.20 (1978) 597–605.
Reinstein, D. K., DeBoissiere, T., Robinson, N., and Wurtman, R. J., Radial maze performance in three strains of mice: role of the fimbria/fornix. Brain Res.263 (1983) 172–176.
Represa, A., Tremblay, E., and Ben-Ary, Y., Aberrant growth of mossy fibers and enhanced kainic acid binding sites induced in rats by early hyperthyroidism. Brain Res.423 (1987) 325–328.
Roderick, T. H., Wimer, R. E., and Wimer, C. C., Genetic manipulation of neuroanatomical traits: in: Knowing, Thinking, and Believing, pp. 143–178. Eds L. Petrinovich and J. L. McGaugh. Plenum Press, New York 1976.
Sadile, A. G., De Luca, B., and Cioffi, A., Long-term habituation to novel environment: amnesic and hyperamnesic effects of various postexposure treatments. Abh. Akad. Wiss. DDR5 (1978) 203–218.
Schwegler, H., Crusio, W. E., Lipp, H.-P., and Heimrich, B., Water-maze learning in the mouse correlates with variation in hippocampal morphology. Behav. Genet.18 (1988) 153–166.
Schwegler, H., and Lipp, H.-P., Is there a correlation between hippocampal mossy fiber distribution and two-way avoidance performance in mice and rats?. Neurosci. Lett.23 (1981) 25–30.
Schwegler, H., and Lipp, H.-P., 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 (1983) 1–39.
Schwegler, H., Lipp, H.-P., and Crusio, W. E., The NZB mouse: hippocampal mossy fiber patterns and behavioral profiles of young and older animals. Drug Dev. Res.15 (1988) 297–305.
Schwegler, H., Lipp, H.-P., Van der Loos, H., and Buselmaier, W., Individual hippocampal mossy fiber distribution in mice correlates with two-way avoidance performance. Science214 (1981) 817–819.
Schüz, A., and Hein, F. M., Comparison between the developmental calendars of the cerebral and cerebellar cortices in a precocial and an altricial rodent, in: Cerebellar Functions, pp. 318–321. Ed. E. Bloedel, Springer, Berlin/Heidelberg 1984.
Smith, R. H., Behavioral measures of drift inMus musculus. Behav. Genet.15 (1985) 483–497.
Sprott, R. L., and Staats, J., Behavioral studies using genetically defined mice. A bibliography. Behav. Genet.5 (1975) 27–82.
Sprott, R. L., and Staats, J., Behavioral studies using genetically defined mice. A bibliography (July 1973–July 1976). Behav. Genet.8 (1978) 183–206.
Sprott, R. L., and Staats, J., Behavioral studies using genetically defined mice. A bibliography (July 1976–August 1978). Behav. Genet.9 (1979) 87–102.
Sprott, R. L., and Staats, J., Behavioral studies using genetically defined mice. A bibliography (August 1978–July 1979). Behav. Genet.10 (1980) 93–104.
Sprott, R. L., and Staats, J., Behavioral studies using genetically defined mice. A bibliography (August 1979–July 1980). Behav. Genet.11 (1981) 73–84.
Stanfield, B. B., and Trice, J. E., Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp. Brain Res.72 (1988) 399–406.
Tauck, D. L., and Nadler, J. V., Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci.5 (1985) 1016–1022.
Timm, F., Zur Histochemie der Schwermetalle, Das Sulfid-Silber-Verfahren. Dtsch. Z. Ges. Gericht. Med.46 (1958) 706–711.
Tolman, E. C., The inheritance of maze-learning ability in rats. J. comp. Psychol.4 (1924) 1–18.
Van Abeelen, J. H. F., Effects of genotype on mouse behavior. Anim. Behav.14 (1966) 218–225.
Van Abeelen, J. H. F., Van der Kroon, P. H., and Bekkers, M. F., Mice selected for rearing behavior: some physiological variables. Behav. Genet.3 (1973) 85–90.
Wahlsten, D., Contribution of the genes (c) and retinal degeneration (rd) to a strain-by-training procedures interaction in avoidance learning in mice. Behav. Genet.3 (1973) 303–316.
Wahlsten, D., Heredity and brain structure, in: Genetics, Environment and Intelligence, pp. 93–115. Ed. A. Oliverio. Elsevier/North Holland, Amsterdam 1977.
Wahlsten, D., Genes with incomplete penetrance and the analysis of brain development, in: Genetics of the Brain, pp. 367–391. Ed. I. Lieblich. Elsevier, Amsterdam 1982.
West, J. R., and Dewey, S. L., Mossy fiber sprouting in the fascia dentata after unilateral entorhinal lesions: quantitative analysis using computer-assisted image processing. Neurosci.13 (1984) 377–384.
West, J. R., and Hodges Savola, C. A., Permanent hippocampal mossy fiber hyperdevelopment following prenatal ethanol exposure. Neurobehav. Toxic. Terat.5 (1983) 139–150.
Wimer, C. C., Correlates of mouse brain weight: a search for component morphological traits, in: Development and Evolution of Brain Size, pp. 147–162. Eds M. E. Hahn, C. Jensen and B. C. Dudek. Academic Press, New York 1979.
Wimer, C. C., Wimer, R. E., and Wimer, J. S., An association between granule cell density in the dentate gyrus and two-way avoidance conditioning in the house mouse. Behav. Neurosci.97 (1983) 844–856.
Wimer, R. E., and Wimer, C. C., Animal behavior genetics: a search for the biological foundations of behavior. A. Rev. Psychol.36 (1985) 171–218.
Wirtshafter, D., and Asin, K. E., Impaired radial maze performance in rats with electrolytic median raphe lesions. Exp. Neurol.79 (1983) 412–421.
Wolfer, D. P., Lipp, H.-P., Leisinger-Trigona, M.-C., and Hausheer-Zarmakupi, Z., Correlations between hippocampal circuitry and behavior: infrapyramidal mossy fibers and navigation in a Morris water maze. Acta anat.128 (1987) 346.
Wolfer, D. P., Lipp, H.-P., Schwegler, H., Brust, M., and Leisinger-Trigona, M.-C., Hippocampal mossy fibers and avoidance learning in mice treated postnatally with corticosterone: correlations with extent and left/right asymmetry. Soc. Neurosci. Abstr.13 (1987) 225.
Wright, S., Evolution in Mendelian populations. Genetics16 (1931) 97–159.
Zar, J. H., Biostatistical Analysis. Prentice-Hall, Englewood Cliffs, N. J. 1974.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lipp, H.P., Schwegler, H., Crusio, W.E. et al. Using genetically-defined rodent strains for the identification of hippocampal traits relevant for two-way avoidance behavior: a non-invasive approach. Experientia 45, 845–859 (1989). https://doi.org/10.1007/BF01954059
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF01954059