Abstract
The nature of place-cell firing in the hippocampus is discussed with relevance to control of discharge characteristics in a “cue-sterile” open-field environment. Although it can be demonstrated that cell firing in this context is controlled by spatial influences, it is also shown that firing within the place field and the location of the place field can be altered by nonspatial influences as well. Within-field firing in this environment is controlled to a large degree by the trajectory of the animal’s movements. Analyses involving forward or backward time shifts in firing, adjusted for variation in speed of movement, trajectory convergence, and number of spikes, produced no indication that complex cell firing reflects either memory for, or anticipated arrival in, locations other than where the cell fired originally. Nor is the location of the place field strictly dependent upon the spatial features of the apparatus, since it is shown that place-cell firing can be changed readily by altering the significance or relevance of a particular location. Place-cell plasticity in this context suggests nonspatial control over where place cells fire. These results are considered in terms of hippocampal cell coding of specific types of spatial information. Considerable discussion is devoted to whether coding of place is shifted in the same cell, or whether there is emergence of place firing by a different cell (detected by the same electrode), as an explanation for this apparent plasticity. Although no resolution is provided, the implications of these findings for a strict spatial mapping theory of the hippocampus are addressed and other interpretations are explored.
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Berger, T. W., Rinaldi, P. C., Weisz, D. J., & Thompson, R. F. (1983). Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. Journal of Neurophysiology, 50, 1197–1219.
Best, P. J., & Ranck, J. B., Jr. (1982). The reliability of the relationship between hippocampal unit activity and sensory-behavioral events in the rat. Experimental Neurology, 75, 652–664.
Best, P. J., & Thompson, L. T. (1984). Hippocampal cells which have place field activity also show changes in activity during classical conditioning. Society for Neuroscience Abstracts, 10, 125.
Best, P. J., & Thompson, L. T. (1989). Persistence, reticence, and opportunism of place-field activity in hippocampal neurons. Psychobiology, 17, 230–235.
Bostock, E., Taube, J., & Muller, R. U. (1988). The effects of head orientation on the firing of hippocampal place cells. Society for Neuroscience Abstracts, 14, 127.
Breese, C. R., Hampson, R. E., & Deadwyler, S. A. (1987). Direction contingent firing of hippocampal place cells. Society for Neuroscience Abstracts, 13, 608.
Breese, C. R., Hampson, R. E., & Deadwyler, S. A. (1988). Significance of spatial location determines the firing characteristics of rat hippocampal place cells. Society for Neuroscience Abstracts, 14, 126.
Breese, C. R., Hampson, R. E., & Deadwyler, S. A. (1989). Hippocampal place cells: Stereotypy and plasticity. Journal of Neuroscience, 9, 1097–1111.
Christian, E. P., & Deadwyler, S. A. (1986). Behavioral functions and hippocampal cell types: Evidence for two nonoverlapping populations in the rat. Journal of Neurophysiology, 55, 331–348.
Eichenbaum, H., & Cohen, N. J. (1988). Representation in the hippocampus: What do hippocampal neurons encode? Trends in Neuroscience, 11, 244–248.
Eichenbaum, H., Kuperstein, M., Fagan, A., & Nagode, J. (1987). Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor discrimination task. Journal of Neuroscience, 7, 716–732.
Foster, T. C., Castro, C. A., & McNaughton, B. L. (1988). Influence of motor set on place-related hippocampal complex spike cell activity. Society for Neuroscience Abstracts, 14, 396.
Foster, T. C., Christian, E. P., Hampson, R. E., Campbell, K. A., & Deadwyler, S. A. (1987). Sequential dependencies regulate sensory evoked responses of single units in the rat hippocampus. Brain Research, 408, 86–96.
Kubie, J. L. (1984). A driveable bundle of microwires for collecting single-unit data from freely moving rats. Physiology & Behavior, 32, 115–118.
Kubie, J. L., Fox, S. E., & Muller, R. U. (1984). Variations in place firing with the state of the hippocampal EEG. Society for Neuroscience Abstracts, 10, 599.
McNaughton, B. L. (1989). Neuronal mechanisms for spatial computation and information storage. In L. Nadel, L. A. Cooper, P. Culicover, & R. Harnish (Eds.), Neural connections and mental computations (pp. 285–350). Cambridge, MA: MIT Press.
McNaughton, B. L., Barnes, C. A., & O’Ceefe, J. (1983). The contributions of position, direction and velocity to single unit activity in the hippocampus of freely moving rats. Experimental Brain Research, 52, 41–49.
McNaughton, B. L., O’Keefe, J., & Barnes, C. A. (1983). The stereotrode: A new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. Journal of Neuroscience Methods, 8, 391–397.
Morris, R. G. M. (1983). An attempt to dissociate “spatial-mapping” and “working-memory” theories of hippocampal function. In W. Seifert (Ed.), Neurobiology of the hippocampus (pp. 405–432). London: Academic Press.
Muller, R. U., & Kubie, J. L. (1986). Introduction of time into the study of place cells. Society for Neuroscience Abstracts, 12, 521.
Muller, R. U., & Kubie, J. L. (1987). The effects of changes in the environment of the spatial firing of hippocampal complex-spike cells. Journal of Neuroscience, 7, 1951–1968.
Muller, R. U., Kubie, J. L., & Ranck, J. B., Jr. (1987). Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. Journal of Neuroscience, 7, 1935–1950.
O’Keefe, J. (1979). A review of the hippocampal place cells. Progress in Neurobiology, 13, 419–439.
O’Keefe, J, & Conway, D. H. (1978). Hippocampal place units in the freely moving rat: Why they fire where they fire. Experimental Brain Research, 31, 573–590.
O’Keefe, J, & Dostrovsky, J. (1971). The hippocampus as a spatial map: Preliminary evidence from unit activity in the freely-moving rat. Brain Research, 34, 171–175.
O’Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Oxford University Press.
O’Keefe, J., & Speakman, A. (1987). Single unit activity in the rat hippocampus during a spatial memory task. Experimental Brain Research, 68, 1–27.
Olton, D. S., Becker, J. T., & Handelmann, G. E. (1979). Hippocampus, space, and memory. Behavioral Brain Science, 2, 313–365.
Olton, D. S., Walker, J. A., & Gage, F. H. (1978). Hippocampal connections and spatial discrimination. Brain Research, 139, 295–308.
Parkinson, J. K., Murray, E. A., & Mishkin, M. (1988). A selective mnemonic role for the hippocampus in monkeys: Memory for the location of objects. Journal of Neuroscience, 8, 4159–4167.
Ranck, J. B., Jr. (1984). Head direction cells in the deep cell layer of dorsal pre-subiculum in freely moving rats. Society for Neuroscience Abstracts, 10, 599.
Rupniak, N. M., & Gaffan, D. (1987). Monkey hippocampus and learning about spatially directed movements. Journal of Neuroscience, 7, 2331–2337.
Taube, J. S., Muller, R. U., & Ranck, J. B., Jr. (1988). Effects of environmental manipulations on the discharge of head-direction cells in the post-subiculum. Society for Neuroscience Abstracts, 14, 126.
Thompson, L. T., & Best, P. J. (1988). Hippocampal place cell to silent cell ratios in freely-behaving rats. Society for Neuroscience Abstracts, 14, 126.
Watanabe, T., & Niki, H. (1985). Hippocampal unit activity and delayed response in the monkey. Brain Research, 325, 241–254.
Wible, C. G., Findling, R. L., Shapiro, M., Lang, E. J., Crane, S., & Olton, D. S. (1986). Mnemonic correlates of unit activity in the hippocampus. Brain Research, 339, 97–110.
Wiener, S. I., & Eichenbaum, H. (1988). Two functional categories of hippocampal complex spike cells. Society for Neuroscience Abstracts, 14, 126.
Zipser, D. (1985). A computational model of hippocampal place fields. Behavioral Neuroscience, 99, 1006–1017.
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This investigation was supported (in part) by Research Scientist Award DA00119 from the ADAMHA awarding institute NIDA, as well as NIDA Grants DA03502 and DA04441 to S.A.D. The efforts of Sonia Stitcher in helping to prepare the manuscript are greatly appreciated.
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Deadwyler, S.A., Breese, C.R. & Hampson, R.E. Control of place-cell activity in an open field. Psychobiology 17, 221–227 (1989). https://doi.org/10.1007/BF03337772
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DOI: https://doi.org/10.1007/BF03337772