Advertisement

Hippocampal Spatial Representations and Navigation in Primates

Abstract

Damage to the temporal lobe that includes the hippocampal formation or to one of its main connection pathways, the fornix, produces amnesia (see Scoville and Milner, 1957; Squire and Knowlton, 1994; Gaffan, 1994). One of the memory deficits in amnesic humans is a major impairment in remembering not just what objects have been seen recently, but also where they have been seen (Smith and Milner, 1981). In experimental studies in monkeys to define the crucial structures to which damage produces memory impairments, it has been shown that hippocampal or fornix damage produces deficits in learning about where objects have been seen, in object-place memory tasks (Parkinson, Murray and Mishkin, 1988; Angeli, Murray and Mishkin, 1993; Gaffan, 1994).

Key word

hippocampus space view place head direction memory monkey presubiculum 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Amari, S. Dynamics of pattern formation in lateral-inhibition type neural fields Biological Cybernetics 1977; 27: 77–87PubMedCrossRefGoogle Scholar
  2. Angeli, S.J., Murray, E.A., Mishkin, M. Hippocampectomized monkeys can remember one place but not two. Neuropsychologia 1993; 31:1021–30PubMedCrossRefGoogle Scholar
  3. Burgess, N., Recce, M., O’Keefe, J. A model of hippocampal function. Neural Networks 1994; 7: 1065–81CrossRefGoogle Scholar
  4. Epstein, R., Kan wisher, N. A cortical representation of the local visual environment. Nature 1998; 392: 598–601PubMedCrossRefGoogle Scholar
  5. Feigenbaum, J.D., Rolls, E.T. Allocentric and egocentric spatial information processing in the hippocampal formation of the behaving primate. Psychobiology 1991; 19: 21–40Google Scholar
  6. Foster, T.C., Castro, CA., McNaughton, B.L. Spatial selectivity of rat hippocampal neurons: Dependence on preparedness for movement. Science 1989; 244:1580–2PubMedCrossRefGoogle Scholar
  7. Gaffan, D. Scene-specific memory for objects: A model of episodic memory impairment in monkeys with fornix transection. J Cogn Neurosci 1994; 6: 305–20CrossRefGoogle Scholar
  8. Georges-François, P., Rolls, E.T., Robertson, R.G. Spatial view cells in the primate hippocampus: Allocentric view not head direction or eye position or place. Cerebral Cortex 1999; 9: 197–212PubMedCrossRefGoogle Scholar
  9. McNaughton, B.L., Barnes, CA., Gerrard, J.L., Gothard, K., Jung, M.W., Knierim, J.J., Kudrimoti, H., Qin, Y., Skaggs, W.E., Suster, M., Weaver, K.L. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 1996; 199: 173–85PubMedGoogle Scholar
  10. Muller, R.U., Ranck, J.B., Taube, J.S. Head direction cells: properties and functional significance. Current Opinion in Neurobiol 1996; 6: 196-206O’Keefe, J., Speakman, A. Single unit activity in the rat hippocampus during a spatial memory task. Exp Brain Res 1987; 68: 1–27Google Scholar
  11. O’Mara, S.M., Rolls, E.T., Berthoz, A., Kesner, R.P. Neurons responding to whole-body motion in the primate hippocampus. J Neurosci 1994; 14: 6511–23PubMedGoogle Scholar
  12. Ono, T., Tamura, R., Nishijo, H., Nakamura, K. ANeural mechanisms of recognition and memory in the limbic system@. In: Brain Mechanisms of Perception and Memory: From Neuron to Behavior, Ono, T., Squire, L.R., Raichle, M.E., Perrett, D.I. and Fukuda, M. eds. Ch 19, pp 330–355. New York: Oxford University Press, 1993.Google Scholar
  13. Parkinson, J.K., Murray, E.A., Mishkin, M. A selective mnemonic role for the hippocampus in monkeys: Memory for the location of objects. J Neurosci 1988; 8: 4059–167Google Scholar
  14. Robertson, R.G., Rolls, E.T., Georges-François, P. Spatial view cells in the primate hippocampus: Effects of removal of view details. J Neurophysiol 1998, 79: 1145–56PubMedGoogle Scholar
  15. Robertson, R.G., Rolls, E.T., Georges-François, P. and Panzeri, S. Head direction cells in the primate pre-subiculum. Hippocampus 1999; 9: 206–19PubMedCrossRefGoogle Scholar
  16. Rolls, E.T. AFunctions of neuronal networks in the hippocampus and neocortex in memory@. in: Neural Models of Plasticity: Experimental and Theoretical Approaches Byrne, J.H., Berry, W.O., eds. Ch 13, pp 240–265. San Diego: Academic Press, 1989.Google Scholar
  17. Rolls, E.T. A theory of hippocampal function in memory. Hippocampus 1996; 6: 601–20PubMedCrossRefGoogle Scholar
  18. Rolls, E.T. (1999) Spatial view cells and the representation of place in the primate hippocampus. Hippocampus 9: 467–80PubMedCrossRefGoogle Scholar
  19. Rolls, E.T. (2001) Neuronal networks, synaptic plasticity, and memory systems in primates. Ch. 10, pp. 224–262 in Neuronal Mechanisms of Memory Formation ed. C. Holscher. Cambridge University Press: Cambridge.Google Scholar
  20. Rolls, E.T., Miyashita, Y., Cahusac, P.M.B., Kesner, R.P., Niki, H., Feigenbaum, J., Bach, L. Hippocampal neurons in the monkey with activity related to the place in which a stimulus is shown. J Neurosci 1989; 9: 1835–45PubMedGoogle Scholar
  21. Rolls, E.T., O’Mara, S.M. View-responsive neurons in the primate hippocampal complex. Hippocampus 1995; 5: 409–24PubMedCrossRefGoogle Scholar
  22. Rolls, E.T., Robertson, R.G., Georges-François, P. Spatial view cells in the primate hippocampus. Eur J Neurosci 1997; 9: 1789–94PubMedCrossRefGoogle Scholar
  23. Rolls, E.T., Treves, A. Neurai Networks and Brain Function. Oxford: Oxford University Press, 1998Google Scholar
  24. Rolls, E.T., Treves, A., Robertson, R.G., Georges-François, P., Panzeri, S. Information about spatial view in an ensemble of primate hippocampal cells. J Neurophysiol 1998; 79: 1797–813PubMedGoogle Scholar
  25. Rolls, E.T., Trappenberg, T.P., Stringer, S.M. (unpublished observations) A network for spatial and episodic memory.Google Scholar
  26. Samsonovich, A., McNaughton, B. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neuroscience 1997; 17: 5900–20Google Scholar
  27. Scoville, W.B., Milner, B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiat 1957; 20: 11–21PubMedCrossRefGoogle Scholar
  28. Smith, M.L., Milner, B. The role of the right hippocampus in the recall of spatial location. Neuropsychologia 1981; 19: 781–93PubMedCrossRefGoogle Scholar
  29. Squire, L.R., Knowlton, B.J. A Memory, hippocampus, and brain systems@. In: the Cognitive Neurosciences Gazzaniga, M. ed. Ch 53, pp 825–837. Cambridge, Mass.: MIT Press, 1994Google Scholar
  30. Stringer, S.M., Trappenberg, T.P., Rolls, E.T., Araujo, I.E.T. (unpublished observations) Self-organising continuous attractor networks and path integration. I. One-dimensional models of head direction cells.Google Scholar
  31. Stringer, S.M., Rolls, E.T., Trappenberg, T.P.,Araujo, I.E.T. (unpublished observations) Self-organising continuous attractor networks and path integration. II. Two-dimensional models of place cells.Google Scholar
  32. Stringer, S.M., Rolls, E.T. (unpublished observations) Self-organising continuous attractor network models of hippocampal spatial view cells.Google Scholar
  33. Taube, J.S., Goodridge, J.P., Golob, E.J., Dudchenko, P.A., Stackman, R.W. Processing the head direction signal: A review and commentary. Brain Res Bull 1996; 40: 477-86PubMedCrossRefGoogle Scholar
  34. Treves, A., Rolls, E.T. A computational analysis of the role of the hippocampus in memory. Hippocampus 1994; 4: 374-9PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  1. 1.Department of Experimental PsychologyUniversity of OxfordOxfordEngland

Personalised recommendations