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The Septohippocampal System and Path Integration

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The Behavioral Neuroscience of the Septal Region

Abstract

An extraordinary contribution of the septum is its influence in synchronizing the electrical activity of the hippocampal formation, a structure that comprises almost a third of the forebrain of the rat. The behavioral relationships of the synchronized patterns of activity, known as the theta rhythm or rhythmical slow activity (RSA), are well known. It is closely coupled to ongoing behavior (Vanderwolf 1969). RSA occurs during locomotion, but it is absent during immobility and many other movements that do not involve locomotion, including licking, chewing, and shivering. In general, the amplitude of theta rhythm is large during large body movements while its frequency increases with forceJvelocity of movement initiation (Whishaw and Vanderwolf 1973; Morris and Hagen 1983). During steady ongoing movements, the theta rhythm has a relatively constant amplitude and frequency that is independent of movement speed. The striking relationship between hippocampal RSA and movement would suggest that the function of the septohippocampal formation is related to movement.

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References

  • Alyan, S., and Jander, R. 1994. Short-range homing in the house mouse, Mus mus-culus: stages in the learning of directions. Animal Behav. 48:285–298.

    Article  Google Scholar 

  • Amaral, D.G., and Witter, M.P. 1995. Hippocampal formation. In The Rat Nervous System., ed. G. Paxinos, pp. 443–493. San Diego: Academic Press.

    Google Scholar 

  • Astur, R.S., Ortiz, M.L., and Sutherland, R. J. 1998. A characterization of performance by men and women in a virtual Morris water task: a large and reliable sex difference. Behav. Brain. Res. 93:185–190.

    Article  PubMed  CAS  Google Scholar 

  • Barlow, J.S. 1964. Inertial navigation as a basis for animal navigation. J. Theor. Biol. 6:76–117.

    Article  PubMed  CAS  Google Scholar 

  • Barnes, C. 1979. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 93:74–104.

    Article  PubMed  CAS  Google Scholar 

  • Barnett, S.S. 1975. The Rat: A Study in Behavior. Chicago: The University of Chicago Press.

    Google Scholar 

  • Blair, H.T., and Sharp, P.E. 1996. Visual and vestibular influences on head direction cells in the anterior thalamus of the rat. Behav. Neurosci. 110:643–660.

    Article  PubMed  CAS  Google Scholar 

  • Chen, L.L., Lin, L.H., Green, E.J., Barnes, C.A., and McNaughton, B.L. 1994. Head direction cells in the rat posterior cortex, I. Anatomical distribution and behavioral modulation. Exp. Brain Res. 101:8–23.

    Article  PubMed  CAS  Google Scholar 

  • Cooper, W.E., and Vitt, L. J. 1986. Tracking of female conspecific odor trains by broad-headed skinks (Eumeces laticeps). Ethology. 7:241–248.

    Google Scholar 

  • Cornetz, V. 1910. Trajets de fourmis et retours au nid. Mém. Inst. Gen. Psychol. 2:1–169.

    Google Scholar 

  • Darwin, C. 1873. Origin of certain instincts. Nature. (Lond) 7:417–418.

    Article  Google Scholar 

  • Eliam, D., and Golani, D. 1989. Home base behavior of rats (Rattus norvegicus) exploring a novel environment. Behav. Brain Res. 34:199–211.

    Article  Google Scholar 

  • Etienne, A.S., Lambert, S. J., Reverdin, B., and Teroni, E. 1993. Learning to recalibrate the role of dead reckoning and visual cues in spatial navigation. Animal Learn. Behav. 21:266–280.

    Article  Google Scholar 

  • Etienne, A.S., Mauer, R., and Saucy, F. 1988. Limitations in the assessment of path dependent information. Behaviour. 106:81–111.

    Article  Google Scholar 

  • Etienne, A.S., Teroni, E., Hurni, C, and Portenierh, V. 1990. The effect of a single light cue on homing behavior of the golden hamster. Animal Behav. 39:17–41.

    Article  Google Scholar 

  • Galef, G.B., Jr. 1980. Diving for food: analysis of a possible case of social learning in wild rats (Rattus norvegicus). J. Comp. Physiol. Psychol. 94:416–425.

    Article  Google Scholar 

  • Gallistel, C.R. 1990. The Organization of Learning. Cambridge, MA: MIT Press.

    Google Scholar 

  • Golob, E.J., and Taube, J.S. 1997. Head direction cells and episodic spatial information in rats without a hippocampus. Proc. Natl. Acad. Sci. USA. 94:7645–7650.

    Article  PubMed  CAS  Google Scholar 

  • Gray, J.A. 1982. The Neuropsychology of Anxiety. Oxford: Clarendon Press.

    Google Scholar 

  • Gray, J.A., and McNaughton, N. 1983. Comparison between the behavioral effects of septal and hippocampal lesions: a review. Neurosci. Biobehav. Rev. 7:119–188.

    Article  PubMed  CAS  Google Scholar 

  • Jung, M.W., and McNaughton, B.L. 1993. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus. 3:165–182.

    Article  PubMed  CAS  Google Scholar 

  • Lashley, K.S. 1951. The problem of serial order in behavior. In Cerebral Mechanisms in Behavior., ed. L.A. Jeffress, pp. 112–136. New York: Wiley.

    Google Scholar 

  • Lubar, J.F., and Numan, R. 1973. Behavioral and physiological studies of septal function and related medial cortical structures. Behav. Biol. 8:1–25.

    Article  PubMed  CAS  Google Scholar 

  • Maaswinkel, H., Jarrard, L.E., and Whishaw, I.Q. In press. Hippocampectomized rats are impaired in homing by path integration. Hippocampus.

    Google Scholar 

  • Maaswinkel, H., and Whishaw, I.Q. 1999. Homing with locale, taxon, and dead reckoning strategies by foraging rats: sensory hierarchy in spatial navigation. Behav. Brain Res. 99:143–152.

    Article  PubMed  CAS  Google Scholar 

  • Maurer, R., and Séguinot, V. 1995. What is modeling for? A critical review of the models of path integration. J. Theor. Biol. 175:457–475.

    Article  Google Scholar 

  • McNaughton, B.L., Barnes, C.A., Gerrard, J.L., Gothard, K., Jung, M.W., Knierm, J.J., et al. 1996. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J. Exp. Biol. 199:173–185.

    PubMed  CAS  Google Scholar 

  • Means, L.W., Hardy, W.T., Gabriel, M., and Uphold, J.D. 1971. Utilization of odor trails by rats in maze learning. J. Comp. Physiol. Psychol. 76:160–164.

    Article  PubMed  CAS  Google Scholar 

  • Mittelsteadt, M.-L., and Glasauer, S. 1991. Idiothetic navigation in gerbils and humans. Zool. Jahrb. Physiol. 95:427–435.

    Google Scholar 

  • Mittelstaedt-Burger, M.L. 1972. Idiothetic course control and visual orientation. In Processing in the Visual System of Arthropods., ed. R. Wehner, pp. 121–130. Berlin: Springer.

    Google Scholar 

  • Mittelsteadt, M.-L., and Mittelsteadt, H. 1980. Homing by path integration in a mammal. Naturwissenschafen. 67:566–567.

    Article  Google Scholar 

  • Mizumori, S.J.Y., and Williams, J.D. 1993. Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J. Neurosci. 13:4015–4028.

    PubMed  CAS  Google Scholar 

  • Morris, R.G.M., Garrud, P., Rawlins, I, and O’Keefe, J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature. 297:681–683.

    Article  PubMed  CAS  Google Scholar 

  • Morris, R.G.M., and Hagan, J.J. 1983. Hippocampal electrical activity and ballistic movement. In Neurobiology of the Hippocampus., ed. W. Seifert, pp. 321–331. New York: Academic Press.

    Google Scholar 

  • Muller, R.U., Stead, M., and Patch, J. 1996. The hippocampus as a cognitive graph. J. Gen. Physiol. 107:663–694.

    Article  PubMed  CAS  Google Scholar 

  • Oddie, S.D., Kirk, I.J., Whishaw, I.Q., and Bland, B.H. 1997. Hippocampal formation is involved in movement selection: evidence from medial septal cholinergic modulation and concurrent slow-wave (theta rhythm) recording. Behav. Brain Res. 88:169–180.

    Article  PubMed  CAS  Google Scholar 

  • Oddie, S.D., Stefaneck, W, Kirk, I.J., and Bland, B.H. 1996. Intraseptal procaine abolishes hypothalamic stimulation-induced wheel-running and hippocampal theta field activity in rats. J. Neurosci. 16:1948–1956.

    PubMed  CAS  Google Scholar 

  • O’Keefe, J. 1978. Place units in the hippocampus of freely moving rat. Exp. Neurol. 51:78–109.

    Article  Google Scholar 

  • O’Keefe, J. 1993. Hippocampus, theta, and spatial memory. Curr. Opin. Neurobiol. 3:917–924.

    Article  PubMed  Google Scholar 

  • O’Keefe, J., and Nadel, L. 1978. The Hippocampus as a Cognitive Map. Oxford: Clarendon Press.

    Google Scholar 

  • Olton, D.S., and Collison, C. 1979. Intramaze cues and “odor trials” fail to direct choice behavior on an elevated maze. Animal Learn. Behav. 7:221–223.

    Article  Google Scholar 

  • Olton, D.S., and Samuelson, R. J. 1976. Remembrance of places passed: spatial memory in rats. J. Exp. Psych.: Animal Behav. Proces. 2:97–116.

    Article  Google Scholar 

  • O’Mara, S., Rolls, E.T., Bertholz, A., and Desner, R.P. 1994. Neurons responding to whole-body motion in the primate hippocampus. J. Neurosci. 14:6511–6523.

    PubMed  Google Scholar 

  • Samsonovich, A., and McNaughton, B.L. 1997. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17:5900–5920.

    PubMed  CAS  Google Scholar 

  • Schallert, T., Day, L.B., Weisend, M., and Sutherland, R. J. 1996. Spatial learning by hippocampal rats in the Morris Water Task. Soc. Neurosci. Abs. 269.6.

    Google Scholar 

  • Sequinot, V., Maurer, R., and Etienne, A.S. 1993. Dead reckoning in a small mammal: the evaluation of distance. J. Comp. Physiol. A. 173:103–113.

    Google Scholar 

  • Sharp, P.E. 1997. Subicular cells generate similar spatial firing patterns in two geometrically and visually distinctive environments: comparison with hippocampal place cells. Behav. Brain Res. 85:71–92.

    Article  PubMed  CAS  Google Scholar 

  • Sharp, P.E., Blair, H.T., Etkin, D., and Tzanetos, D.B.J. 1995. Influences of vestibular and visual information on the spatial firing patterns of hippocampal place cells. J. Neurosci. 15:173–189.

    PubMed  CAS  Google Scholar 

  • Sutherland, R. J., and Dyck, R. 1984. Place navigation by rats in a swimming pool. Can. J. Psych. 38:322–347.

    Article  Google Scholar 

  • Sutherland, R. J., Whishaw, I.Q., and Kolb, B. 1982. Spatial mapping: definitive disruption by hippocampal or medial frontal cortical damage in the rat. Neurosci. Lett. 31:271–276.

    Article  PubMed  CAS  Google Scholar 

  • Taube, J.S. 1995. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 15:70–85.

    PubMed  CAS  Google Scholar 

  • Taube, J.S., and Burton, H.L. 1995. Head direction cell activity monitored in a novel environment and during a cue conflict situation. J. Neurophysiol. 74:1953–1971.

    PubMed  CAS  Google Scholar 

  • Taube, J.S., Muller, R.U., and Ranck, J.P. 1990. Head direction cells recorded from the postsubiculum in freely moving rats.I. description and quantitative analysis. J. Neurosci. 10:420–435.

    PubMed  CAS  Google Scholar 

  • Vanderwolf, C.H. 1969. Hippocampal electrical activity and voluntary movement in the rat. Electroenceph. Clin. Neurophysiol. 26:407–418.

    Article  PubMed  CAS  Google Scholar 

  • Whishaw, I.Q. 1985. Formation of a place learning-set by the rat: a new paradigm for neurobehavioral studies. Physiol. Behav. 35:979–1005.

    Article  Google Scholar 

  • Whishaw, I.Q. 1991. Latent learning in a swimming pool place task by rats: evidence for the use of associative and not cognitive mapping processes. Q. J. Exp. Psychol. B. 43:83–103.

    PubMed  CAS  Google Scholar 

  • Whishaw, I.Q. 1998. Place learning in hippocampal rats and the path integration hypothesis. Neurosci. Biobehav. Rev. 22:209–220.

    Article  PubMed  CAS  Google Scholar 

  • Whishaw, I.Q., Cassel, J.-C, and Jarrard, L. 1995. Rats with fimbria-fornix lesions display a place response in a swimming pool: a dissociation between getting there and knowing where. J. Neurosci. 15:5779–5788.

    PubMed  CAS  Google Scholar 

  • Whishaw, I.Q., Coles, B.K.L., and Bellerive, C.H.M. 1995. Food carrying: a new method for naturalistic studies of spontaneous and forced alternation. J. Neurosci. Meth. 61:139–143.

    Article  CAS  Google Scholar 

  • Whishaw, I.Q., and Jarrard, L. 1995. Similarities vs. difference in place learning and circadian activity in rats after fimbria-fornix section or ibotenate removal of hippocampal cells. Hippocampus. 5:595–604.

    Article  PubMed  CAS  Google Scholar 

  • Whishaw, I.Q., and Jarrard, L. 1996. Evidence for extrahippocampal involvement in place learning and hippocampal involvement in path integration. Hippocampus. 6:513–524.

    Article  PubMed  CAS  Google Scholar 

  • Whishaw, I.Q., and Mittleman, G. 1987. Visits to starts, routes and places by rats (Rattus norvegicus) in swimming pool navigation tasks. J. Comp. Psychol. 100: 422–431.

    Article  Google Scholar 

  • Whishaw, I.Q., and Tomie, J. 1997. Piloting and dead reckoning dissociated by fimbria-fornix lesions in a rat food carrying task. Behav. Brain Res. 89:87–97.

    Article  PubMed  CAS  Google Scholar 

  • Whishaw, I.Q., and Tomie, J. 1997. Perseveration on place reversals in spatial swimming pool tasks: further evidence for place learning in hippocampal rats. Hippocampus. 7:361–370.

    Article  PubMed  CAS  Google Scholar 

  • Whishaw, I.Q., and Vanderwolf, C.H. 1973. Hippocampal EEG and behaviour: changes in amplitude and frequency of RSA (Theta rhythm) associated with spontaneous and learned movement patterns in rats and cats. Behav. Biol. 8:461–484.

    Article  PubMed  CAS  Google Scholar 

  • Whishaw, I.Q., and Whishaw, G.E. 1996. Nonspecific aggression influences food carrying: studies on a wild population of Rattus norvegicus. Agg. Behav. 22:47–66.

    Article  Google Scholar 

  • Wiener, S.I. 1996. Spatial behavioral and sensory correlates of hippocampal CA1 complex spike cell activity: implications for information processing functions. Prog. Neurobiol. 49:335–361.

    PubMed  CAS  Google Scholar 

  • Worden, R. 1992. Navigation by fragment fitting: a theory of hippocampal function. Hippocampus. 2:165–188.

    Article  PubMed  CAS  Google Scholar 

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Whishaw, I.Q. (2000). The Septohippocampal System and Path Integration. In: Numan, R. (eds) The Behavioral Neuroscience of the Septal Region. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-1302-4_11

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  • DOI: https://doi.org/10.1007/978-1-4612-1302-4_11

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