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## Place cell discharge is extremely variable during individual passes of the rat through the firing field. Proc Natl Acad Sci U (1998)

Venue: | S A |

Citations: | 15 - 1 self |

### BibTeX

@ARTICLE{Fenton98placecell,

author = {André A Fenton and Robert U Muller},

title = {Place cell discharge is extremely variable during individual passes of the rat through the firing field. Proc Natl Acad Sci U},

journal = {S A},

year = {1998},

pages = {3182--3187}

}

### OpenURL

### Abstract

ABSTRACT The idea that the rat hippocampus stores a map of space is based on the existence of ''place cells'' that show ''location-specific'' firing. The discharge of place cells is confined with remarkable precision to a cell-specific part of the environment called the cell's ''firing field.'' We demonstrate here that firing is not nearly as reliable in the time domain as in the positional domain. Discharge during passes through the firing field was compared with a model with Poisson variance of the location-specific firing determined by the time-averaged positional firing rate distribution. Place cells characteristically fire too little or too much compared with expectations from the random model. This fundamental property of place cells is referred to as ''excess firing variance'' and has three main implications: (i) Place cell discharge is not only driven by the summation of many small, asynchronous excitatory synaptic inputs. (ii) Place cell discharge may encode a signal in addition to the current head location. (iii) The excess firing variance helps explain why the errors in computing the rat's position from the simultaneous activity of many place cells are large. How do rodents solve difficult spatial problems? On behavioral grounds, it is believed that rats (and mice) can form map-like representations of their surroundings. Once such a representation is formed, the rat can use it to navigate because the representation contains information about the overall layout or geometry of the surroundings (1-3). Given that a spatial map exists, it is natural to ask how it is organized in the nervous system. That is, where is the map located and how does it operate? Our current understanding of spatial maps is based on the discovery of hippocampal place cells 25 years ago (4). It was observed that individual neurons in the hippocampus (pyramidal cells of CA3 and CA1) (5) show ''location-specific'' firing. A given place cell discharges rapidly only when a rat's head is in a certain part of the environment. Outside this ''firing field'' region, the cell rarely discharges This appealing picture is predicated on a tacit assumptionthat in addition to firing only when the head is in the firing field, that a place cell fires in much the same way each time the head goes through the field along much the same path. It is not uncommon, however, for a robust place cell to be silent as the rat's head passes through the center of its firing field (8). Such failures to discharge are seen even if there was substantial firing on other, nearly identical passes. The purpose of this paper is to demonstrate that such ''excess variance'' of firing is characteristic of place cells. One way to demonstrate this would be to show that decreases in firing from a maximum are not well predicted by how much a path deviates from the path that produces the maximum firing. Unfortunately, this procedure cannot be used because the differences between pairs of passes do not satisfy the triangular inequality requirement of a metric that estimates the difference between two passes. Thus, there is no unambiguous way to decide how much two paths differ and therefore no way to predict the firing along one path from the firing along another. A stochastic method therefore was used to characterize the excess variance. Specifically, the number of spikes observed during complete passes through the firing field was compared with the number of spikes expected from the time-averaged firing rates in the sequence of pixels encountered during the pass. A pass begins when the rat's head enters the firing field and ends when the head leaves the field. Thus, we neglected all processes that occur on a time scale shorter than a pass, which is about a second. In doing so, we ignored at least one known source of firing modulation, namely, the 5-10 Hz theta rhythm (9, 10). This omission is justified because a pass lasts many theta cycles, so the effects of theta modulation average out. What constraints are there on the method of predicting the number of spikes during a pass using only the sequence of head positions and the time-averaged firing rates at those positions? Because we are interested in demonstrating the excess variance, we chose the model that produces the greatest variance of spike number for any given pass. This choice maximizes the difficulty of rejecting the null hypothesis, that the observed firing is predictable from head position and the time averaged positional rate pattern. This decision dictates the use of an inhomogeneous Poisson process (IPP). In general, an IPP is a time series of ordinary Poisson processes such that the rate parameter for each ordinary Poisson process is adjusted according to the current state of the system. For instance, an IPP can be used to estimate the number of events registered by a radiation detector as the position of the detector is moved relative a radiation source. In the present case, the rate parameter for each ordinary Poisson process in the IPP is set to the time- The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked ''advertisement'' in accordance with 18 U.S.C. §1734 solely to indicate this fact.