Reactivation of Hippocampal Cell Assemblies: Effects of Behavioral State, Experience, and EEG Dynamics

Abstract

During slow wave sleep (SWS), traces of neuronal activity patterns from preceding behavior can be observed in rat hippocampus and neocortex. The spontaneous reactivation of these patterns is manifested as the reinstatement of the distribution of pairwise firing-rate correlations within a population of simultaneously recorded neurons. The effects of behavioral state [quiet wakefulness, SWS, and rapid eye movement (REM)], interactions between two successive spatial experiences, and global modulation during 200 Hz electroencephalographic (EEG) "ripples" on pattern reinstatement were studied in CA1 pyramidal cell population recordings. Pairwise firing-rate correlations during often repeated experiences accounted for a significant proportion of the variance in these interactions in subsequent SWS or quiet wakefulness and, to a lesser degree, during SWS before the experience on a given day. The latter effect was absent for novel experiences, suggesting that a persistent memory trace develops with experience. Pattern reinstatement was strongest during sharp wave-ripple oscillations, suggesting that these events may reflect system convergence onto attractor states corresponding to previous experiences. When two different experiences occurred in succession, the statistically independent effects of both were evident in subsequent SWS. Thus, the patterns of neural activity reemerge spontaneously, and in an interleaved manner, and do not necessarily reflect persistence of an active memory (i.e., reverberation). Firing-rate correlations during REM sleep were not related to the preceding familiar experience, possibly as a consequence of trace decay during the intervening SWS. REM episodes also did not detectably influence the correlation structure in subsequent SWS, suggesting a lack of strengthening of memory traces during REM sleep, at least in the case of familiar experiences.

The hippocampal debate: are we asking the right questions?

“…Non-spatial hippocampal correlates can be explained. Place cell recordings are examining detailed quantitative second-order properties of the tuning curves, including both spatial [39,112,151,174,208] (to list only a few) and non-spatial [11,94,247], and these properties are being modeled at a quantitative level [16,172,196,205]. Detailed explanations of hippocampal roles in both spatial and non-spatial tasks are available [72,173,196,225].…”

“…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.…”

“…One state, called theta, shows a profound 7 -10 Hz rhythm [150,229] with a higher 40 Hz rhythm (called gamma) riding above it [18] and occurs during movement and other attentive behaviors [229]. During theta, cellular activity tends to be smooth; a relatively constant proportion of hippocampal pyramidal cells fire spikes, with each cell firing on the order of a second or two [94,150,169]. The other state, called LIA (large-amplitude irregular activity) shows a noisier EEG punctuated by occasional 100 ms sharp-wa6es with a 200 Hz rhythm riding on them [25,150,229,249].…”

“…The other state, called LIA (large-amplitude irregular activity) shows a noisier EEG punctuated by occasional 100 ms sharp-wa6es with a 200 Hz rhythm riding on them [25,150,229,249]. Cellular activity in LIA is usually quiet, with strong bursts of activity during the sharp-waves [25,94,150,169]. Place fields are only seen during theta states; during LIA states, cells fire during sharp-waves, independent of the location of the animal [94,150].…”

“…Cellular activity in LIA is usually quiet, with strong bursts of activity during the sharp-waves [25,94,150,169]. Place fields are only seen during theta states; during LIA states, cells fire during sharp-waves, independent of the location of the animal [94,150]. The theories that predicted replay of hippocampal states during sleep suggest that information is written into hippocampus during theta and read out during LIA [24,102,215].…”