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Level of Arousal During the Small Irregular Activity State in the Rat Hippocampal EEG

Department of Neuroscience and Center for the Neural Basis of Cognition, University of Pittsburgh, Pittsburgh, Pennsylvania 15260

Submitted 6 November 2003; accepted in final form 20 January 2004

The sleeping rat cycles between two well-characterized hippocampal physiological states, large irregular activity (LIA) during slow-wave sleep (SWS) and theta activity during rapid-eye-movement sleep (REM). A third, less well-characterized electroencephalographic (EEG) state, termed "small irregular activity" (SIA), has been reported to occur when an animal is startled out of sleep without moving and during active waking when it abruptly freezes. We recently found that the hippocampal population activity of a spontaneous sleep state whose EEG resembles SIA reflects the rat's current location in space, suggesting that it is also a state of heightened arousal. To test whether this spontaneous SIA state corresponds to the SIA state reported in the literature and to compare the level of arousal during SIA to the other well-characterized physiological states, we recorded unit activity from ensembles of hippocampal CA1 pyramidal cells, EEG from the hippocampus and the neocortex, and electromyography (EMG) from the dorsal neck musculature in rats presented with auditory stimuli while foraging for randomly scattered food pellets and while sleeping. Auditory stimuli presented during sleep reliably induced SIA episodes very similar to spontaneous SIA in hippocampal and neocortical EEG amplitudes and power spectra, EMG amplitude, and CA1 population activity. Both spontaneous and elicited SIA exhibited neocortical desynchronization, and both had EMG amplitude comparable to that of waking LIA. We conclude based on this and other evidence that spontaneous SIA and elicited SIA correspond to a single state and that the level of arousal in SIA is higher than in the well-characterized sleep states but lower than the active theta state.

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