Hippocampus place cell discharge is an important model system for understanding cognition, but evidence is missing that the place code is under the kind of dynamic attentional control characterized in primates as selective activation of one neural representation and suppression of another, competing representation. We investigated the apparent noise ("overdispersion") in the CA1 place code, hypothesizing that overdispersion results from discharge fluctuations as spatial attention alternates between distal cues and local/self-motion cues. The hypothesis predicts that: (1) preferential use of distal cues will decrease overdispersion; (2) global, attention-like states can be decoded from ensemble discharge such that both the discharge rates and the spatial firing patterns of individual cells will be distinct in the two states; (3) identifying attention-like states improves reconstructions of the rat's path from ensemble discharge. These predictions were confirmed, implying that a covert, dynamic attention-like process modulates discharge on a ϳ1 s time scale. We conclude the hippocampus place code is a dynamic representation of the spatial information in the immediate focus of attention.

The assumption that hippocampal place cells (PCs) form the neural substrate of cognitive maps can be experimentally tested by comparing the effect of experimental interventions on PC activity and place navigation. Conditions that interfere with place navigation (darkness, cholinergic blockade) but leave PC activity unaffected obviously disrupt spatial memory at a post-PC level. Situations creating a conf lict between egocentric and allocentric orientation (place navigation in the Morris water maze filled with slowly rotating water) slow down spatial learning. PC recording in rats searching food pellets in a rotating arena makes it possible to determine which firing fields are stable relative to the room (allocentrically dependent on sighted extramaze landmarks), to the surface of the arena (dependent on egocentric path integration mechanisms and intra-arena cues), or disappear during rotation. Such comparison is made possible by the computerized tracking system simultaneously displaying a rat's locomotion and the respective firing rate maps both in the room reference and arena reference frames. More severe conf lict between allocentric and egocentric inputs is produced in the field clamp situation when the rat searching food in a ring-shaped arena is always returned by rotation of the arena to the same allocentric position. Ten-minute exposure to this condition caused subsequent disintegration or remapping of 70% PCs (n ‫؍‬ 100). Simultaneous examination of PC activity and navigation is possible in the place avoidance task. A rat searching food in a stationary or rotating arena learns to avoid an allocentrically or egocentrically defined location where it receives mild electric footshock. In the place preference task the rat releases pellet delivery by entering an unmarked goal area and staying in it for a criterion time. Both tasks allow direct comparison of the spatial reference frames used by the PCs and by the behaving animal.The invitation to write an inaugural article is a unique opportunity to combine a review of what has been done with a program statement describing how we want to continue our research, explaining the philosophy of our approach, and discussing its specific tools. We should like to stress from the outset that the article does not represent an individual but a research team, the ever changing composition of which is not a weakness but a source of strength. HistoryThe present Laboratory of Neurophysiology of Memory of the Institute of Physiology of the Academy of Sciences in Prague was organized in 1958 with the aim to study nonimpulse forms of neural communication. The research concentrated on the analysis of cortical spreading depression (1), which was at the time the best known example of a neurohumoral phenomenon propagating over the entire brain surface of laboratory rodents. From the very beginning this mainly electrophysiological project lead to behavioral investigations when Buresova (2) proposed to use repeated waves of spreading depression as a functional ablation procedur...

Navigation by means of cognitive maps appears to require the hippocampus; hippocampal place cells (PCs) appear to store spatial memories because their discharge is con¢ned to cell-speci¢c places called ¢ring ¢elds (FFs). Experiments with rats manipulated idiothetic and landmark-related information to understand the relationship between PC activity and spatial cognition. Rotating a circular arena in the light caused a discrepancy between these cues. This discrepancy caused most FFs to disappear in both the arena and room reference frames. However, FFs persisted in the rotating arena frame when the discrepancy was reduced by darkness or by a card in the arena. The discrepancy was increased by`¢eld clamping' the rat in a room-de¢ned FF location by rotations that countered its locomotion. Most FFs dissipated and reappeared an hour or more after the clamp. Place-avoidance experiments showed that navigation uses independent idiothetic and exteroceptive memories. Rats learned to avoid the unmarked footshock region within a circular arena. When acquired on the stable arena in the light, the location of the punishment was learned by using both room and idiothetic cues; extinction in the dark transferred to the following session in the light. If, however, extinction occurred during rotation, only the arena-frame avoidance was extinguished in darkness; the room-de¢ned location was avoided when the lights were turned back on. Idiothetic memory of room-de¢ned avoidance was not formed during rotation in light; regardless of rotation, there was no avoidance when the lights were turned o¡, but room-frame avoidance reappeared when the lights were turned back on. The place-preference task rewarded visits to an allocentric target location with a randomly dispersed pellet. The resulting behaviour alternated between random pellet searching and target-directed navigation, making it possible to examine PC correlates of these two classes of spatial behaviour. The independence of idiothetic and exteroceptive spatial memories and the disruption of PC ¢ring during rotation suggest that PCs may not be necessary for spatial cognition; this idea can be tested by recordings during the place-avoidance and preference tasks.

Continuous rotation of an arena in a cue-rich room dissociates the stationary room-bound information from the rotating arenabound information. This disrupted spatial discharge in the majority of place cells from rats trained to collect randomly scattered food. In contrast, most place cell firing patterns recorded from rats trained to solve a navigation task on the rotating arena were preserved during the rotation. Spatial discharge was preserved in both the task-relevant stationary and the task-irrelevant rotating reference frames, but firing was more organized in the taskrelevant frame. It is concluded that, (i) the effects of environmental manipulations can be understood with confidence only when the rat's purposeful behavior is used to formulate interpretations of the data, and (ii) hippocampal place cell activity is organized in multiple overlapping spatial reference frames.