Experimental Brain Research

, Volume 58, Issue 1, pp 11–28 | Cite as

Dissociation between components of spatial memory in rats after recovery from the effects of retrohippocampal lesions

  • F. Schenk
  • R. G. M. Morris


1. A series of 4 experiments examined the performance of rats with retrohippocampal lesions on a spatial water-maze task. 2. The animals were trained to find and escape onto a hidden platform after swimming in a large pool of opaque water. The platform was invisible and could not be located using olfactory cues. Successful escape performance required the rats to develop strategies of approaching the correct location with reference solely to distal extramaze cues. 3. The lesions encompassed the entire rostro-caudal extent of the lateral and medial entorhinal cortex, and included parts of the pre- and para-subiculum, angular bundle and subiculum. Groups ECR 1 and 2 sustained only partial damage of the subiculum, while Group ECR+S sustained extensive damage. These groups were compared with sham-lesion and unoperated control groups. 4. In Expt 1A, a profound deficit in spatial localisation was found in groups ECR 1 and ECR+S, the rats receiving all training postoperatively. In Expt 1B, these two groups showed hyperactivity in an open-field. In Expt 2, extensive preoperative training caused a transitory saving in performance of the spatial task by group ECR 2, but comparisons with the groups of Expt 1A revealed no sustained improvement, except on one measure of performance in a post-training transfer test. All rats were then given (Expt 3) training on a cueing procedure using a visible platform. The spatial deficit disappeared but, on returning to the normal hidden platform procedure, it reappeared. Nevertheless, a final transfer test, during which the platform was removed from the apparatus, revealed a dissociation between two independent measures of performance: the rats with ECR lesions failed to search for the hidden platform but repeatedly crossed its correct location accurately during traverses of the entire pool. This partial recovery of performance was not (Expt 4) associated with any ability to discriminate between two locations in the pool. 5. The apparently selective recovery of aspects of spatial memory is discussed in relation to O'Keefe and Nadel's (1978) spatial mapping theory of hippocampal function. We propose a modification of the theory in terms of a dissociation between procedural and declarative sub-components of spatial memory. The declarative component is a flexible access system in which information is stored in a form independent of action. It is permanently lost after the lesion. The procedural component is “unmasked” by the retrohippocampal lesion giving rise to the partial recovery of spatial localisation performance.

Key words

Spatial memory Water maze Hippocampus Entorhinal cortex Recovery of function 


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  1. Andersen P (1975) Organisation of hippocampal interneurones and their interconnections. In: Isaacson RL, Pribram KH (eds) The hippocampus, Vol 1. Plenum Press, New York, 1975Google Scholar
  2. Beckstead RM (1978) Afferent connections of the entorhinal area in the rat as demonstrated by retrograde cell labelling with horseradish peroxidase. Brain Res 152: 249–264Google Scholar
  3. Cohen NJ (1984) Preserved learning capacity in amnesia: evidence for multiple memory systems. In: Butters N, Squire LR (eds) The neuropsychology of memory. Guilford Press, New YorkGoogle Scholar
  4. Cohen NJ, Squire LR (1980) Preserved learning capacity and retention of pattern-analysing skill in amnesia: dissociation of knowing how and knowing that. Science 210: 207–210PubMedGoogle Scholar
  5. Dickinson A (1980) Contemporary animal learning theory. Cambridge University Press, CambridgeGoogle Scholar
  6. Finger S, Stein DG (1982) Brain damage and recovery. Academic Press, New YorkGoogle Scholar
  7. Gaile GL, Burt JE (1980) Directional statistics. University of East Anglia Press, NorwichGoogle Scholar
  8. Gray JA (1982) The neuropsychology of anxiety. Oxford University Press, OxfordGoogle Scholar
  9. Handelmann GE, Olton DS (1981) Spatial memory following damage to the Hippocampal CA3 pyramidal cells with kainic acid: impairment and recovery with preoperative training. Brain Res 217: 41–58Google Scholar
  10. Handelmann GE, Olton DS, O'Donohue TL, Bennfield MC, Jacobowitz DM, Cummins CJ (1983) Effects of time and experience on hippocampal neurochemistry after damage to the CA3 subfield. Pharmacol Biochem Behav 18: 551–561Google Scholar
  11. Hjorth-Simonsen A, Jeune B (1972) Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J Comp Neurol 144: 215–232Google Scholar
  12. Jarrard LE (1978) Selective hippocampal lesions: differential effects on performance by rats of a spatial task with preoperative vs. postoperative training. J Comp Physiol Psychol 92: 1119–1127Google Scholar
  13. Jarrard LE (1983) Selective hippocampal lesions and behaviour: effects of kainic acid lesions on performance of place and cue tasks. Behav Neurosci 97: 873–889Google Scholar
  14. Kolb B, Sutherland RJ, Whishaw IQ (1983) A comparison of the contributions of frontal and parietal association cortex to spatial localisation in rats. Behav Neurosci 97: 13–27Google Scholar
  15. Kohler C, Sundberg H (1977) Locomotor activity and exloratory behaviour after dorsal entorhinal cortex lesions in the albino rat. Behav Biol 20: 419–432Google Scholar
  16. Lasher SS, Steward O (1981) The time-course of changes in open-field activity following bilateral entorhinal lesions in rats and cats. Behav Neurol Biol 32: 1–20Google Scholar
  17. LeVere TE (1975) Neural stability, sparing and behavioural recovery following brain damage. Psychol Rev 82: 344–358Google Scholar
  18. LeVere ND, LeVere TE (1982) Recovery of function after brain damage: support for the compensation theory of the behavioural deficit. Physiol Psychol 10: 165–174Google Scholar
  19. Liu CN, Chambers WW (1958) Intraspinal sprouting of dorsal root axons. Arch Neurol Psychiat 79: 46–61Google Scholar
  20. Loesche J, Steward O (1977) Behavioural correlates of denervation and reinnervation of the hippocampal formation of the rat: recovery of alternation performance following unilateral entorhinal cortex lesions. Brain Res Bull 2: 31–39Google Scholar
  21. Meibach RC, Siegel A (1975) The origin of fornix fibers which project to the mammillary bodies in the rat: a horseradish peroxidase study. Brain Res 88: 508–512Google Scholar
  22. Morris RGM (1981) Spatial localisation does not depend upon the presence of local cues. Learn Motiv 12: 239–260Google Scholar
  23. Morris RGM (1983) An attempt to dissociate “spatial mapping” and “working-memory” theories of hippocampal function. In: Siefert W (ed) The neurobiology of the hippocampus. Academic Press, LondonGoogle Scholar
  24. Morris RGM (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Meth 11: 47–60Google Scholar
  25. Morris RGM, Garrud P, Rawlins JNP, O'Keefe J (1982) Place-navigation impaired in rats with hippocampal lesions. Nature 297: 681–683Google Scholar
  26. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, OxfordGoogle Scholar
  27. Olton DS (1983) Memory functions of the hippocampus. In: Siefert W (ed) The neurobiology of the hippocampus. Academic Press, LondonGoogle Scholar
  28. Olton DS, Walker JA, Gage FH (1978) Hippocampal connections and spatial discrimination. Brain Res 139: 295–308Google Scholar
  29. Ramirez JJ, Stein DG (1984) Sparing and recovery of spatial alternation performance after entorhinal cortex lesions in rats. Behav Brain Res 13: 53–61Google Scholar
  30. Schapiro S, Salas N, Vukovich K (1970) Hormonal effects on ontogeny of swimming ability in the rat: assessment of central nervous system development. Science 168: 147–151Google Scholar
  31. Schenk F (1983) Activity and exploratory behaviour after lesions of the medial entorhinal cortex in the woodmouse (Apodemus sylvaticus). Behav Neural Biol 37: 89–107Google Scholar
  32. Simson EL, Jones AP, Gold RM (1981) Horizontal stereotaxic atlas of the albino rat brain. Brain Res Bull 6: 297–326Google Scholar
  33. Squire LR, Zola-Morgan S (1983) The neurology of memory: the case for correspondence between the findings for man and non-human primates. In: Deutsch JA (ed) The physiological basis of memory (2nd edn.) Academic Press, New YorkGoogle Scholar
  34. Steward O (1976) Topographic organisation of the projections from the entorhinal area to the hippocampal formation of the rat. J Comp Neurol 167: 285–314Google Scholar
  35. Steward O, Loesche J, Horton WC (1977) Behavioural correlates of denervation and reinnervation of the hippocampal formation of the rat: open field activity and cue utilisation following bilateral antorhinal cortex lesions. Brain Res Bull 2: 41–48Google Scholar
  36. Sutherland RJ, Whishaw IQ, Kolb B (1983) A behavioural analysis of spatial localisation following electrolytic, kainateor colchicine-induced damage to the hippocampal formation in the rat. Behav Brain Res 7: 133–153Google Scholar
  37. Suzuki S, Augerinos G, Black AH (1980) Stimulus control of spatial behaviour on the eight-arm maze in rats. Learn Motiv 11: 1–18Google Scholar
  38. Swanson LW, Cowan WM (1977) An autoradiographic study of the organisation of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172: 49–84Google Scholar
  39. Van-Hoesen GW (1982) The para-hippocampal gyrus — new observations regarding its cortical connections in the monkey. Trends Neurosci 5: 345–350Google Scholar
  40. Vanderwolf CH, Leung LWS (1983) Hippocampal slow activity: a brief history and the effects of entorhinal lesions and phencyclidine. In: Siefert W (ed) The neurobiology of the hippocampus. Academic Press, LondonGoogle Scholar
  41. Weiskrantz L, Warrington EK (1975) The problem of the amnesic syndrome in man and animals. In: Isaacson RL, Pribram KH (eds) The hippocampus, Vol 2. Plenum Press, New YorkGoogle Scholar
  42. Winocur G, Breckenridge CB (1973) Cue-dependent behaviour of hippocampally damaged rats in a complex maze. J Comp Physiol Psychol 82: 512–522Google Scholar
  43. Wyss JM (1981) Autoradiographic study of the efferent connections of entorhinal cortex in the rat. J Comp Neurol 199: 495–512Google Scholar

Copyright information

© Springer-Verlag 1985

Authors and Affiliations

  • F. Schenk
    • 1
  • R. G. M. Morris
    • 2
  1. 1.Institut de PhysiologieUniversité de LausanneLausanneSwitzerland
  2. 2.MRC Cognitive Neuroscience Group, Psychological LaboratoryUniversity of St. AndrewsSt. AndrewsScotland

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