Hippocampal place cells are not controlled by visual input during the small irregular activity state in the rat

In the actively foraging rat, hippocampal pyramidal cells have strong spatial correlates. Each "place cell" fires rapidly only when the rat enters a particular delimited portion of its environment, called the "place field" of that cell. Hippocampal pyramidal cells also exhibit spatial selectivity during a physiological state that occurs during sleep, termed "small irregular activity" (SIA), because of the appearance of the hippocampal EEG. It is not known whether rats determine their current location in space during SIA using current visual information or whether they recall the location in which they fell asleep. To address this question, we recorded spikes from ensembles of CA1 pyramidal cells and hippocampal EEG while rats slept along the edge of a large circular recording arena with minimal local features in a room with prominent distal visual cues. To move the rats to a new location in the room while they were sleeping, we slowly rotated the recording arena on which they slept to a new orientation in the room. Hippocampal place cell activity in subsequent SIA episodes reflected the location in the room in which the rats fell asleep, rather than the location to which they were moved, although the alignment of the rats' spatial map was governed by the room cues in the subsequent active foraging session. Thus, the hippocampal population activity during SIA does not result from the processing of current visual information but instead probably reflects a memory for the location in which the rat fell asleep.