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 (Fig. 1A). The precise confinement of discharge to firing fields at once suggested that the hippocampus is a key component of the map and that mapping information is in part positional information. In this view, the rat's current location is signaled by the conjoint firing of a set of place cells. As the rat moves, its head leaves the field of some cells and enters the field of others, so that the across-cell firing pattern changes in a characteristic way. It thus is presumed that the rat's head position can be accurately calculated if the current across-cell discharge pattern is known (6, 7).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 fie...