Skip to main content

Hippocampal Spatial Representations and Navigation in Primates

  • Chapter
The Neural Basis of Navigation

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).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Amari, S. Dynamics of pattern formation in lateral-inhibition type neural fields Biological Cybernetics 1977; 27: 77–87

    Article  PubMed  Google Scholar 

  • Angeli, S.J., Murray, E.A., Mishkin, M. Hippocampectomized monkeys can remember one place but not two. Neuropsychologia 1993; 31:1021–30

    Article  PubMed  Google Scholar 

  • Burgess, N., Recce, M., O’Keefe, J. A model of hippocampal function. Neural Networks 1994; 7: 1065–81

    Article  Google Scholar 

  • Epstein, R., Kan wisher, N. A cortical representation of the local visual environment. Nature 1998; 392: 598–601

    Article  PubMed  Google Scholar 

  • Feigenbaum, J.D., Rolls, E.T. Allocentric and egocentric spatial information processing in the hippocampal formation of the behaving primate. Psychobiology 1991; 19: 21–40

    Google Scholar 

  • Foster, T.C., Castro, CA., McNaughton, B.L. Spatial selectivity of rat hippocampal neurons: Dependence on preparedness for movement. Science 1989; 244:1580–2

    Article  PubMed  Google Scholar 

  • Gaffan, D. Scene-specific memory for objects: A model of episodic memory impairment in monkeys with fornix transection. J Cogn Neurosci 1994; 6: 305–20

    Article  Google Scholar 

  • 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: 197–212

    Article  PubMed  Google Scholar 

  • 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: 173–85

    PubMed  Google Scholar 

  • 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: 1–27

    Google Scholar 

  • 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: 6511–23

    PubMed  Google Scholar 

  • 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 

  • 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: 4059–167

    Google Scholar 

  • 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: 1145–56

    PubMed  Google Scholar 

  • Robertson, R.G., Rolls, E.T., Georges-François, P. and Panzeri, S. Head direction cells in the primate pre-subiculum. Hippocampus 1999; 9: 206–19

    Article  PubMed  Google Scholar 

  • 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 

  • Rolls, E.T. A theory of hippocampal function in memory. Hippocampus 1996; 6: 601–20

    Article  PubMed  Google Scholar 

  • Rolls, E.T. (1999) Spatial view cells and the representation of place in the primate hippocampus. Hippocampus 9: 467–80

    Article  PubMed  Google Scholar 

  • 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 

  • 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: 1835–45

    PubMed  Google Scholar 

  • Rolls, E.T., O’Mara, S.M. View-responsive neurons in the primate hippocampal complex. Hippocampus 1995; 5: 409–24

    Article  PubMed  Google Scholar 

  • Rolls, E.T., Robertson, R.G., Georges-François, P. Spatial view cells in the primate hippocampus. Eur J Neurosci 1997; 9: 1789–94

    Article  PubMed  Google Scholar 

  • Rolls, E.T., Treves, A. Neurai Networks and Brain Function. Oxford: Oxford University Press, 1998

    Google Scholar 

  • 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: 1797–813

    PubMed  Google Scholar 

  • Rolls, E.T., Trappenberg, T.P., Stringer, S.M. (unpublished observations) A network for spatial and episodic memory.

    Google Scholar 

  • Samsonovich, A., McNaughton, B. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neuroscience 1997; 17: 5900–20

    Google Scholar 

  • Scoville, W.B., Milner, B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiat 1957; 20: 11–21

    Article  PubMed  Google Scholar 

  • Smith, M.L., Milner, B. The role of the right hippocampus in the recall of spatial location. Neuropsychologia 1981; 19: 781–93

    Article  PubMed  Google Scholar 

  • 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, 1994

    Google Scholar 

  • 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 

  • 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 

  • Stringer, S.M., Rolls, E.T. (unpublished observations) Self-organising continuous attractor network models of hippocampal spatial view cells.

    Google Scholar 

  • 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: 477-86

    Article  PubMed  Google Scholar 

  • Treves, A., Rolls, E.T. A computational analysis of the role of the hippocampus in memory. Hippocampus 1994; 4: 374-9

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Edmund T. Rolls .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Springer Science+Business Media New York

About this chapter

Cite this chapter

Rolls, E.T. (2002). Hippocampal Spatial Representations and Navigation in Primates. In: Sharp, P.E. (eds) The Neural Basis of Navigation. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0887-8_10

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-0887-8_10

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-5288-4

  • Online ISBN: 978-1-4615-0887-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics