The Cholinergic Septo-Hippocampal Pathway, Learning and Memory

  • Robert Jaffard
  • Daniel Galey
  • Jacques Micheau
  • Thomas Durkin
Part of the Advances in Behavioral Biology book series (ABBI, volume 28)

Abstract

This paper summarizes the results of parallel behavioral, neurochemical and pharmacological experiments aimed at studying the role of septo-hippocampal cholinergic neurones in learning and memory processes in mice. A large body of evidence from pharmacological experiments supports the association of central cholinergic mechanisms with many aspects of behavior (De Feudis, 1974) and in particular with information encoding storage and/or retrieval (Deutsch, 1971; Biederman, 1974; Matthies, 1974; Squire and Davis, 1981). The hypothesis that the hippocampus plays a key role in memory processes (Isaacson, 1974) has focussed considerable attention on the possibility that the cholinergic neurones of the septo-hippocampal pathway (Lewis and Shute, 1967) may mediate control on some mechanisms involved in mnemonic function (Routtenberg, 19S4). To circumvent the difficulties deriving from the frequently used approach of pharmacological studies utilising peripheral drug injections which have often generated discordant results on this problem, we have adopted the research strategy of investigating the modulation of learning and memory processes in selected inbred mouse strains combined with direct neurochemical methods to investigate hippocampal cholinergic activity.

Keywords

Choline Acetylcholine Acetyl Haloperidol Crest 

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References

  1. Bartus, R.T., Dean, R.L., Beer, B., and Lippa, A.S., 1982, The cholinergic hypothesis of geriatric memory dysfunction, Science, 217:408.CrossRefGoogle Scholar
  2. Biederman, G.B., 1974, The search for the chemistry of memory. Recent trends and the logic of investigation in the role of cholinergic and adrenergic transmitters, Progr. Neurobiol., 2:291.CrossRefGoogle Scholar
  3. Costa, E., Panula, P., Thompson, H., and Cheney, D., 1983, The transsynaptic regulation of the septal-hippocampal cholinergic neurones, Life Sci., 32:165.CrossRefGoogle Scholar
  4. De Feudis, F.V., 1974, “Central cholinergic systems and behavior”. Academic Press, London.Google Scholar
  5. Destrade, C., 1981, Effects of post-trial hypothalamic stimulation driving two types of hippocampal rhythmical slow activity (RSA) on memory processes in mice, Neurosci. Lett., 7:236.Google Scholar
  6. Destrade, C., and Cardo, B., 1974, Effects of post-trial hippocampal stimulation on time-dependent improvement of performance in mice, Brain Res., 78:447.CrossRefGoogle Scholar
  7. Destrade, C., Soumireu-Mourat, B., and Cardo, B. 1973, Effects of post-trial hippocampal stimulation on acquisition of operant behavior in the mouse, Behav. Biol., 8:713.CrossRefGoogle Scholar
  8. Deutsch, J.A., 1971, The cholinergic synapses and the site of memory, Science, 174:788.CrossRefGoogle Scholar
  9. Douglas, R.J., 1972, Pavlovian conditioning and the brain, In: “Inhibition and learning”, R.A. Boakes and M.S. Halliday, eds., Academic Press, London.Google Scholar
  10. Durkin, T., Ayad, G., Ebel, A., and Mandel, P., 1977, Regional acetylcholine turnover rates in the brains of three inbred strains of mice: correlations with some interstrain behavioral differences, Brain Res., 136:475.CrossRefGoogle Scholar
  11. Durkin, T., Hashem-Zadeh, H., Mandel, P., Kempf, J., and Ebel, A., 1983, Genotypic variation in the dopaminergic inhibitory control of striatal and hippocampal cholinergic activity in mice, Pharmacol. Biochem. Behav., 19:63.CrossRefGoogle Scholar
  12. Galey, D., Jeantet, Y., Destrade, C., and Jaffard, R., 1983, Facilitation of memory consolidation by post-training electrical stimulation of the medial septal nucleus: Is it mediated by changes in rhythmic slow activity? Behav. Neural Biol., 38:240.CrossRefGoogle Scholar
  13. Galey, D., Durkin, T., Sifakis, G., and Jaffard, R., 1984, Amélioration de conduites spatiales spontanées et acquises après lésion des afférences dopaminergiques septales chez la souris: relations possibles avec l’activité cholinergique hippocampique, C.R.Acad.Sci. Paris, Série III, in press.Google Scholar
  14. Isaacson, R.L. and Kimble, D.P., 1972, Lesions of the limbic system: their effects upon hypotheses and frustration. Behav. Biol., 7:767.CrossRefGoogle Scholar
  15. Jaffard, R., 1978, “Mécanismes cholinergiques hippocampiques associés aux processus d’apprentissage et de mémorisation: Etude comportementale et neurochimique sur trois lignées de souris consanguines”. Thèse de Doctorat d’Etat, Université Bordeaux I.Google Scholar
  16. Jaffard, R. and Destrade, C., 1982, Learning and memory processes as related to genotypic or experimental variations of hippocampal cholinergic activity in inbred strains of mice. in “The Genetics of the Brain”. I. Lieblich, Ed., Elsevier Biomedical Press, Amsterdam.Google Scholar
  17. Jaffard, R. and Galey, D., 1980, Retention of appetitive operant conditioning in mice as a function of training-to-test interval: Effects of pretest electrical stimulation of the hippocampus. Physiol. Behav., 25:845.CrossRefGoogle Scholar
  18. Jaffard, R., Ebel, A., Destrade, C., Ayad, G., Mandel, P. and Cardo, B., 1976, The role of hippocampal cholinergic mechanisms in the acquisition of a bar-press response. Pharmacol. Biochem. Behav., 5:371.CrossRefGoogle Scholar
  19. Jaffard, R., Destrade, C., Soumireu-Mourat, B. and Cardo, B., 1974, Time-dependent improvement of performance on appetitive tasks in mice. Behav. Biol., 11:89.CrossRefGoogle Scholar
  20. Jaffard, R., Destrade, C., Durkin, T. and Ebel, A., 1979, Memory formation as related to genotypic or experimental variations of hippocampal cholinergic activity in mice. Physiol. Behav., 22:1093.CrossRefGoogle Scholar
  21. Jaffard, R., Destrade, C., Soumireu-Mourat, B., Durkin, T. and Ebel, A. 1980, Changes in hippocampal cholinergic activity following learning in mice. Neurosci. Lett., 19:349.CrossRefGoogle Scholar
  22. Jaffard, R., Ebel, A., Destrade, C., Durkin, T., Mandel, P. and Cardo, B., 1980, Effects of hippocampal electrical stimulation on long-term memory and on cholinergic mechanisms in three inbred strains of mice. Brain Res., 133:277.CrossRefGoogle Scholar
  23. Landfield, P.W., 1977, Different effects of post-trial driving or blocking of the theta rhythm on avoidance learning in rats. Physiol. Behav., 18:439–445.CrossRefGoogle Scholar
  24. Lewis, P.R. and Shute, C.C.D., 1967, The cholinergic limbic system: Projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system and the subfornical organ and supraoptic crest. Brain, 90:521.CrossRefGoogle Scholar
  25. Matthies, H., 1974, The biochemical basis of learning and memory. Life Sci., 15:2017.CrossRefGoogle Scholar
  26. Matthies, H., Rauca, C. and Liebmann, H., 1974, Changes in acetylcholine content of different brain regions of the rat during a learning experiment. J. Neurochem., 23:1109.CrossRefGoogle Scholar
  27. McGaugh, J.L., 1966, Time-dependent processes in memory storage. Science, 153:1351.CrossRefGoogle Scholar
  28. Micheau, J., Destrade, C., Jaffard, R. and Caudarella, M., 1983, Effects of physostigmine on memory deficits induced by pretraining electrical stimulation of the dorsal hippocampus in mice. Communication at 13th annual meeting of Society for Neuroscience, Boston, Ma, Nov. 6–11, 1983. Soc. Neurosci. Abstr., V.9, part. 2, p. 826.Google Scholar
  29. Raaijmakers, W.G.M., 1978, Active avoidance learning and choline uptake in rat hippocampal synaptosomes. Neurosci.Lett., suppl.1, 86.Google Scholar
  30. Roberts, W.A. and Dale, R.H., 1981, Remembrance of places lasts: proactive inhibition and patterns of choice in rat spatial memory. Learning and Motivation, 12:261.CrossRefGoogle Scholar
  31. Robinson, S., Malthe-Sorenssen, D., Wood, P. and Commissiong, J., 1979, Dopaminergic control of the septal-hippocampal cholinergic pathway. J. Pharmacol. Exp. Ther., 208:476.Google Scholar
  32. Routtenberg, A., 1972, Memory as an input-output reciprocity: An integrative neurobiological theory. Ann. N.Y. Acad. Sci., 193:159.CrossRefGoogle Scholar
  33. Routtenberg, A., 1984, The CA3 pyramidal cell in the hippocampus: site of intrinsic expression and extrinsic control of memory formation. in “Neuropsychology of memory”, L.R. Squire and N. Butters, Eds, The Guilford Press, New York.Google Scholar
  34. Squire, L.R. and Davis, H.P., 1981, The pharmacology of memory: a neurobiological perspective. Ann. Rev. Pharmacol. Toxicol., 21:323.CrossRefGoogle Scholar
  35. Sutherland, R.J., Whishaw, I.Q. and Regehr, J.C., 1982, Cholinergic receptor blockade impairs spatial localization by use of distal cues in the rat. J. comp. physiol. Psychol., 96:563.CrossRefGoogle Scholar
  36. Teitelbaum, H., Lee, J.F. and Johannessen, J.N., 1975, Behaviorally evoked hippocampal theta waves: A cholinergic response. Science, 188:1114.CrossRefGoogle Scholar
  37. Vanderwolf, C.H., Kramis, R. and Robinson, T.E., 1978, Hippocampal electrical activity during waking behavior and sleep: Analysis using centrally acting drugs. in: Ciba Foundation Symposium 58 (new series), “Functions of the septo-hippocampal system”. Elsevier Excerpta Medica, North-Holland, Amsterdam.Google Scholar
  38. Wetzel, W., Ott, T. and Matthies, H., 1977, Post-training hippocampal rhythmic slow activity (theta) elicited by septal stimulation improves memory consolidation in rats. Behav. Biol., 21:32.CrossRefGoogle Scholar
  39. Wood, P., Cheney, D. and Costa, E., 1979, An investigation of whether septal y-aminobutyrate-containing interneurones are involved in the reduction in the turnover rate of acetylcholine elicited by substance P and ß-endorphin in the hippocampus. Neuroscience, 4:1479.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1985

Authors and Affiliations

  • Robert Jaffard
    • 1
  • Daniel Galey
    • 1
  • Jacques Micheau
    • 1
  • Thomas Durkin
    • 1
  1. 1.Laboratoire de Psychophysiologie, L.A. CNRS no 339Université de Bordeaux ITalence CedexFrance

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