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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1997 Oct 29;352(1360):1505–1513. doi: 10.1098/rstb.1997.0137

Variable place-cell coupling to a continuously viewed stimulus: evidence that the hippocampus acts as a perceptual system.

A Rotenberg 1, R U Muller 1
PMCID: PMC1692048  PMID: 9368939

Abstract

A key feature of perception is that the interpretation of a single, continuously available stimulus can change from time to time. This aspect of perception is well illustrated by the use of ambiguous figures that can be seen in two different ways. When people view such a stimulus they almost universally describe what they are seeing as jumping between two states. If it is agreed that this perceptual phenomenon is causally linked to the activity of nerve cells, the state jumps would have to occur in conjunction with changes in neural activity somewhere in the nervous system. Our experiments suggest that hippocampal place cells are part of a perceptual system. We conducted variations of a 'cue-card rotation' experiment on rats in which the angular position of a prominent visual stimulus on the wall of cylinder is changed in the rat's presence. The three main results are that (i) place-cell firing fields remain stationary if the cue is rotated by 180 degrees, so the relation between the cue and the field is altered; (ii) firing fields rotate by 45 degrees when the cue is rotated by 45 degrees, so the relation between the field and the card is maintained; and (iii) if the cue is first rotated by 180 degrees and then rotated in a series of 45 degrees steps, the field winds up at a different angular position relative to the card when the card is back in its original position. Thus, place cells can fire in two different ways in response to a continuously viewed stimulus. We conclude that place cells reveal that the hippocampal mapping system also has properties expected of a perceptual system.

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Selected References

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  1. Bostock E., Muller R. U., Kubie J. L. Experience-dependent modifications of hippocampal place cell firing. Hippocampus. 1991 Apr;1(2):193–205. doi: 10.1002/hipo.450010207. [DOI] [PubMed] [Google Scholar]
  2. Fox S. E., Ranck J. B., Jr Localization and anatomical identification of theta and complex spike cells in dorsal hippocampal formation of rats. Exp Neurol. 1975 Oct;49(1 Pt 1):299–313. doi: 10.1016/0014-4886(75)90213-7. [DOI] [PubMed] [Google Scholar]
  3. Gómez C., Argandoña E. D., Solier R. G., Angulo J. C., Vázquez M. Timing and competition in networks representing ambiguous figures. Brain Cogn. 1995 Nov;29(2):103–114. doi: 10.1006/brcg.1995.1270. [DOI] [PubMed] [Google Scholar]
  4. Hill A. J. First occurrence of hippocampal spatial firing in a new environment. Exp Neurol. 1978 Nov;62(2):282–297. doi: 10.1016/0014-4886(78)90058-4. [DOI] [PubMed] [Google Scholar]
  5. Kubie J. L. A driveable bundle of microwires for collecting single-unit data from freely-moving rats. Physiol Behav. 1984 Jan;32(1):115–118. doi: 10.1016/0031-9384(84)90080-5. [DOI] [PubMed] [Google Scholar]
  6. Kubie J. L., Muller R. U., Bostock E. Spatial firing properties of hippocampal theta cells. J Neurosci. 1990 Apr;10(4):1110–1123. doi: 10.1523/JNEUROSCI.10-04-01110.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Logothetis N. K., Schall J. D. Neuronal correlates of subjective visual perception. Science. 1989 Aug 18;245(4919):761–763. doi: 10.1126/science.2772635. [DOI] [PubMed] [Google Scholar]
  8. Long G. M., Toppino T. C., Mondin G. W. Prime time: fatigue and set effects in the perception of reversible figures. Percept Psychophys. 1992 Dec;52(6):609–616. doi: 10.3758/bf03211697. [DOI] [PubMed] [Google Scholar]
  9. Markus E. J., Barnes C. A., McNaughton B. L., Gladden V. L., Skaggs W. E. Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus. 1994 Aug;4(4):410–421. doi: 10.1002/hipo.450040404. [DOI] [PubMed] [Google Scholar]
  10. McNaughton B. L., Barnes C. A., Gerrard J. L., Gothard K., Jung M. W., Knierim J. J., Kudrimoti H., Qin Y., Skaggs W. E., Suster M. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol. 1996 Jan;199(Pt 1):173–185. doi: 10.1242/jeb.199.1.173. [DOI] [PubMed] [Google Scholar]
  11. Muller R. U., Kubie J. L., Ranck J. B., Jr Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci. 1987 Jul;7(7):1935–1950. doi: 10.1523/JNEUROSCI.07-07-01935.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Muller R. U., Kubie J. L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci. 1987 Jul;7(7):1951–1968. doi: 10.1523/JNEUROSCI.07-07-01951.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. O'Donnell B. F., Hendler T., Squires N. K. Visual evoked potentials to illusory reversals of the necker cube. Psychophysiology. 1988 Mar;25(2):137–143. doi: 10.1111/j.1469-8986.1988.tb00976.x. [DOI] [PubMed] [Google Scholar]
  14. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971 Nov;34(1):171–175. doi: 10.1016/0006-8993(71)90358-1. [DOI] [PubMed] [Google Scholar]
  15. O'Keefe J. Place units in the hippocampus of the freely moving rat. Exp Neurol. 1976 Apr;51(1):78–109. doi: 10.1016/0014-4886(76)90055-8. [DOI] [PubMed] [Google Scholar]
  16. Quirk G. J., Muller R. U., Kubie J. L. The firing of hippocampal place cells in the dark depends on the rat's recent experience. J Neurosci. 1990 Jun;10(6):2008–2017. doi: 10.1523/JNEUROSCI.10-06-02008.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ranck J. B., Jr Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol. 1973 Nov;41(2):461–531. doi: 10.1016/0014-4886(73)90290-2. [DOI] [PubMed] [Google Scholar]
  18. Sharp P. E., Blair H. T., Etkin D., Tzanetos D. B. Influences of vestibular and visual motion information on the spatial firing patterns of hippocampal place cells. J Neurosci. 1995 Jan;15(1 Pt 1):173–189. doi: 10.1523/JNEUROSCI.15-01-00173.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sharp P. E., Kubie J. L., Muller R. U. Firing properties of hippocampal neurons in a visually symmetrical environment: contributions of multiple sensory cues and mnemonic processes. J Neurosci. 1990 Sep;10(9):3093–3105. doi: 10.1523/JNEUROSCI.10-09-03093.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Taube J. S., Burton H. L. Head direction cell activity monitored in a novel environment and during a cue conflict situation. J Neurophysiol. 1995 Nov;74(5):1953–1971. doi: 10.1152/jn.1995.74.5.1953. [DOI] [PubMed] [Google Scholar]
  21. Wilson M. A., McNaughton B. L. Dynamics of the hippocampal ensemble code for space. Science. 1993 Aug 20;261(5124):1055–1058. doi: 10.1126/science.8351520. [DOI] [PubMed] [Google Scholar]

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