The firing of hippocampal place cells predicts the future position of freely moving rats

Direct observation and automatic, video-based methods reveal that a large fraction of hippocampal pyramidal neurons recorded from freely moving rats behave as “place cells”; the firing of each place cell occurs almost exclusively when the rat is in a restricted part of its current environment. In earlier work, 2-dimensional firing distributions for place cells over the apparatus area were made under the assumption that the correct location for each spike was the animal's position at the instant that the spike was fired. Spatial firing distributions generated in this way often have a very simple structure, in which the single region of intense activity has a just one maximum, and where the rate decreases monotonically in all directions away from the maximum. We will refer to patterns of this sort as “ideal.” We describe how the spatial firing pattern is altered by assigning spikes to positions earlier or later than the instant at which they were fired. Spatial firing distributions were generated for a range of constant displacements of the spike time-series against the position time series. Three quantitative measures were used to estimate the extent to which the spatial firing pattern at different “spike/position shifts” approximated the ideal pattern. The 3 measures are in agreement that spikes must precede the animal's position by about 120 msec for the spatial firing pattern to be closest to the ideal. These results suggest that hippocampal unit activity predicts the animal's future location on a short time scale.

[1]  V. B. Domesick Projections from the cingulate cortex in the rat. , 1969, Brain research.

[2]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[3]  R. F. Thompson,et al.  Neuronal substrate of classical conditioning in the hippocampus , 1976, Science.

[4]  A. Siegel,et al.  Efferent connections of the hippocampal formation in the rat , 1977, Brain Research.

[5]  T W Berger,et al.  Identification of pyramidal cells as the critical elements in hippocampal neuronal plasticity during learning. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[6]  J. O’Keefe A review of the hippocampal place cells , 1979, Progress in Neurobiology.

[7]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[8]  K. E. Sørensen Ipsilateral projection from the subiculum to the retrosplenial cortex in the guinea pig , 1980, The Journal of comparative neurology.

[9]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[10]  Bryan Kolb,et al.  Spatial mapping: definitive disruption by hippocampal or medial frontal cortical damage in the rat , 1982, Neuroscience Letters.

[11]  R. F. Thompson,et al.  Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. , 1983, Journal of neurophysiology.

[12]  W. B. Orr,et al.  Hippocampectomy selectively disrupts discrimination reversal conditioning of the rabbit nictitating membrane response , 1983, Behavioural Brain Research.

[13]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[14]  J. Kubie A driveable bundle of microwires for collecting single-unit data from freely-moving rats , 1984, Physiology & Behavior.

[15]  L. Swanson The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[16]  L. Swanson,et al.  Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  J. Houk,et al.  Correlation and spectral analysis of relations between single unit discharge and muscle activities , 1987, Journal of Neuroscience Methods.

[18]  J. B. Ranck,et al.  Spatial firing patterns of hippocampal complex-spike cells in a fixed environment , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.