Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes

Abstract

Rat hippocampal (CA1) complex spike "place cells" of freely behaving rats were recorded in pairs continuously during a series of waking (exploration and still-alert), drowsy (quiet-awake), and sleeping (slow-wave, pre-rapid-eye-movement and rapid-eye-movement sleep) behaviors. Pairs of units were selected that had nonoverlapping place fields. The rats were restricted from entering the place field of either cell overnight, and on the day of recording cells were exposed to their individual place fields independently and in a counterbalanced manner. Following exposure, recordings were made in the subsequent sleep episodes and the firing characteristics of both cells were analyzed. Following exposure, significant increases in the spiking activity of the exposed cell were observed in the subsequent sleeping states that were not evident in the unexposed cell. The increased activity was observed in the rate of firing (spikes/sec), the rate of occurrence of bursts with multiple spikes, as well as the number of bursts displaying short (2-4 msec) interspike intervals. The findings suggest that neuronal activity of hippocampal place cells in the awake states may influence the firing characteristics of these cells in subsequent sleep episodes. The increased firing rates along with the greater number of multiple spike bursts and the shorter interspike intervals within the burst, following exposure to a cell's place field, may represent possible information processing during sleep.

Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience

“…The foregoing observations of granule cells in hippocampal FD are qualitatively similar to those of pyramidal cells in hippocampal CA1 (Kudrimoti et al 1997;Pavlides and Winson 1989;Qin et al 1997;Skaggs and McNaughton 1996;Wilson and McNaughton 1994). The increased pair-wise correlation and temporal bias are consistent with an underlying associative synaptic modification through a temporally asymmetric LTP-like mechanism at some stage in the system.…”

“…The overall theory that the hippocampus participates in the consolidation process during sleep has recently gained support from studies of place-specific firing of hippocampal CA1 pyramidal neurons. Pavlides and Winson (1989) first observed that if a rat is confined, for a significant amount of time, in the place field of one of the cells being recorded from, the firing rate of that cell is increased during subsequent slow-wave sleep (SWS). Wilson and McNaughton (1994) found that when large numbers of hippocampal cells were simultaneously recorded, the firing rate correlations of cell pairs with overlapping place fields during a spatial task were significantly enhanced during the sleep immediately after the spatial experience.…”

Memory consolidation during sleep: a neurophysiological perspective

“…Using pairs of pyramidal cells, Pavlides and Winson (1989) found that activation of a member of the pair by exposing the rat to the place field of the neuron resulted in increased discharge of that cell in the subsequent sleep epoch (see also Buzsa ki 1996). Wilson and McNaughton (1994) failed to observe increased firing of spatially active neurons during slow wave sleep.…”

The hippocampal debate: are we asking the right questions?

“…There is now strong evidence that hippocampal representations active during awake states are replayed during subsequent sleep states [94,139,161,206,241]. This has been taken as evidence for a hippocampal role in consolidation.…”

“…There is also some evidence for replay of representations during REM sleep as well [96,161,164]. Intriguingly, replay of familiar and novel memories occur at different phases of the theta rhythm: novel memories are replayed at the peak of REM-theta, while familiar memories are replayed at the trough [164].…”