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UCSD COGS 107B - Spatial Firing Patterns of Hippocampal Complex-Spike Cells

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The Journal of Neuroscience, July 1987, 7(7): 1935-l 950 Spatial Firing Patterns of Hippocampal Complex-Spike Cells in a Fixed Environment Robert U. Muller, John L. Kubie, and James B. Ranck, Jr. Departments of Physiology and Anatomy and Cell Biology, Downstate Medical Center (SUNY), Brooklyn, New York 11203 A TV/computer technique was used to simultaneously track a rat’s position in a simple apparatus and record the firing of single hippocampal complex-spike neurons. The primary finding is that many of these neurons behave as “place cells,” as first described by O’Keefe and Dostrovsky (1971) and O’Keefe (1976). Each place cell fires rapidly only when the rat is in a delimited portion of the apparatus (the cell’s “firing field”). In agreement with O’Keefe (1976) and many other authors, we have seen that the firing of place cells is highly correlated with the animal’s position and is remark- ably independent of other aspects of the animal’s behavioral state. Several properties of firing fields were characterized. Fir- ing fields are stable over long time intervals (days) if the environment is constant. They come in several shapes when the animal is in a cylindrical apparatus; moreover, the set of field shapes is different when the animal is in a rectangular apparatus. It also seems that a single cell may have more than one field in a given apparatus. By collecting a sample of 40 place cells in a fixed environment, it has been possible to describe certain features of the place cell population, including the spatial distribution of fields within the appa- ratus, the average size of fields, and the “intensity” of fields (as measured by maximum firing rate). We also tested the hypothesis that the firing rate of each place cell signals the animal’s distance from a point (the field center) so that a weighted average of the firing of the individual cells encodes the animal’s position within the apparatus. The animal’s po- sition, calculated according to this “distance hypothesis,” is systematically different from the animal’s true position; this implies that the hypothesis in its simplest form is wrong. The hippocampal place cells discovered by O’Keefe and Dos- trovsky (197 1) and more fully characterized by O’Keefe (1976) are named for their property of firing rapidly only when a freely moving rat is in a limited region of the space accessible to the animal; this region will be called the cell’s “firing field.” As a result of the large difference between in-field and out-of-field Received Mar. 17, 1986; revised Dec. 1, 1986; accepted Jan. 8, 1987. This work was supported by NIH Grants NS 20686 to J.L.K. and R.U.M and NS 14497 to J.B.R., Jr. We are indebted to Mr. Bobby Marsh of the Department of Physiology for designing and building the interface that allows the animal’s position to be tracked and encoded as a binary number that can be sent to a computer. We thank Dr. Elizabeth Bostock for experimental contributions, Dr. Steven E. Fox for much help and encouragement, and Drs. John O’Keefe and David Ziuser for maw useful discussions. Correspondence should be addressed to Dr. Robert Muller, Department of Physiology-Box 3 1, Downstate Medical Center, 450 Clarkson Avenue, Brooklyn, NY 11203. Copyright 0 1987 Society for Neuroscience 0270-6474/87/071935-16$02.00/O firing, simply watching a rat’s position while monitoring the spikes generated by a cell is sufficient to get a good first impres- sion of the location of a field. For this reason, the authors of most previous studies of place cells have been justified in using their own impressions of the existence and location of firing fields. Unfortunately, a good deal of this work has been less than convincing to individuals who have not directly seen place cell recordings. The first purpose of the work presented here was therefore to document the place cell phenomenon, using auto- matic means for locating the animal and simultaneously re- cording the firing of a place cell. The video-based method lo- cated the rat 60 times/set in a 64 x 64 grid of small rectangular picture elements (pixels) of the video field, so that the raw data consisted of a time series of locations and a parallel time series of action potentials. Video/computer methods for locating the animal have been previously employed by O’Keefe (198 3) and McNaughton et al. (1983a). The location and spike series were used to generate time- averaged, spatial distributions for the cell’s firing rate by divid- ing the total number of spikes fired in each pixel by the total time the rat spent in that pixel. The spatial firing distributions can be inspected for the presence of firing fields by transforming them into color-coded maps of firing rate as a function of po- sition. Firing rate maps are useful for determining, for example, the number of firing fields for a cell or for describing field shapes. A natural extension of documenting the existence of firing fields is characterizing some of their properties. Numerical values for other field properties, such as area or location within the ap- paratus, can be directly derived from the spatial firing rate. These methods will be used to describe average field properties for the place cell population. Most individuals who “listen” to a place cell while observing a rat agree that firing does not occur in association with any special activity on the rat’s part. Best and Ranck (1982) made this point by showing that naive viewers of videotapes with spike data on the sound track chose location as the best correlate of firing. A second purpose of the present work was to measure place cell firing in a reduced behavioral situation, in order to reinforce the idea that place cell firing is “location-specific” rather than “behavior-specific.” The optimal activity pattern would be for the rat to move constantly at the same speed, and to visit all parts of the recording chamber equally often, as would


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UCSD COGS 107B - Spatial Firing Patterns of Hippocampal Complex-Spike Cells

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