Evocation in paradoxical sleep of a hippocampal conditioned cellular response acquired during waking

Abstract

This experiment was a test ofthe possibility that a conditioned hippocampal response acquired during wakefulness could be evoked during paradoxical sleep (PS). After one session of habituation to a tone, waking rats underwent conditioning in four sessions during which the tone was used as the conditioned stimulus preceding a footshock. Pseudoconditioned animals received unpaired tone-shock presentations. There was a 24-h intersession interval. After each session, the same tone, never awakening the animal, was presented during PS phases. Hippocampal multiunit activity (MUA) was analyzed at each tone presentation during waking and during PS. Before conditioning, tone presentation did not affect MUA. During conditioning sessions, it elicited sustained increases in hippocampal discharge. When the tone was presented during postlearning PS, it induced a short-Iasting increase in MUA. On the other hand, in the pseudoconditioned animals, hippocampal activity failed to show any change in response to the tone, whether during wakefulness or during PS. These results suggest that a behaviorally significant stimulus can be recognized during PS.

Appetitive conditioning-induced plasticity is expressed during paradoxical sleep in the medial geniculate, but not in the lateral amygdala.

“…Second, a heart rate conditioned response, acquired in wakefulness through an auditory fear-conditioning procedure, was evoked in PS in response to a conditioned tone (Maho & Hennevin, 1999). Last, supporting the above data, electrophysiological studies have shown that neurons in the hippocampus (Maho, Hennevin, Hars, & Poincheval, 1991), the medial geniculate nucleus (MG; Hennevin, Maho, Hars, & Dutrieux, 1993), and the lateral nucleus of the amygdala (LA; Hennevin, Maho, & Hars, 1998) exhibited enhanced tone responses during PS after the tone had been paired with footshock during wakefulness. This set of results thus demonstrates that learning-induced neuronal changes are maintained and can be expressed during PS.…”

Learning-induced plasticity in the medial geniculate nucleus is expressed during paradoxical sleep.

“…To account for the efficacy of cuing, we must assume that the cue stimulus has been detected during PS. This assumption has been corroborated by electrophysiological studies which have shown that a hippocampal conditioned cellular response acquired during wakefulness can be evoked by presentation of the conditioned stimulus (CS) in PS (Maho, Hennevin, Hars, & Poincheval, 1991). Thus, all of these studies indicate that sensory input is not simply suppressed or ignored by the CNS in PS.…”

Conditioned salivation and associated dreams from REM sleep.

“…In animals and humans, previous research has provided evidence both for (Oniana & Lortkipanidze, 1984; Sasaki & Yoshii, 1984; Maho & Bloch, 1992; Maho et al, 1991; Hennevin & Hars, 1992; Hennevin et al, 1993), and against (Matsumoto et al, 1968; McDonald et al, 1975; Halperin & Iorio, 1981) conditioned reflexes during REM sleep. The results from the present study provide support for the notion that classically conditioned salivary responses can be elicited from REM sleep in humans.…”

“…Blocking REM sleep after learning also impedes subsequent performance (Smith & Butler, 1982; Smith & Kelly, 1988). Similarly, it has been shown that, if a specific CS (such as a tone or ear shock) is used during avoidance training in rats and this same stimulus is then presented during after-training REM sleep, significant task improvement is subsequently observed (Hennevin & Hars, 1987; Hars & Hennevin, 1990, Maho, Hennevin & Hars, 1991). These contingent cueing studies suggest that associative memory processing, at some level, must be occurring during subsequent REM sleep.…”

“…Although several papers have demonstrated the feasibility of eliciting conditioned responses during sleep in both animals and humans (Rowland, 1957; Ikeda, 1991; Ikeda & Morotomi, 1996), there are inconsistencies in whether such responses can (Oniana & Lortkipanidze, 1984; Sasaki & Yoshii, 1984; Maho & Bloch, 1992; Maho, Hennevin, Hars, & Poincheval, 1991; Hennevin & Hars, 1992; Hennevin, Maho, Hars, & Dutrieux, 1993) or cannot (Matsumoto, Miyoshi, & Kooyama, 1968; McDonald, Schicht, Frazier, Shallenberger, & Edwards, 1975; Halperin & Iorio, 1981) be elicited during REM sleep. In related findings, researchers have found prolonged increases in paradoxical sleep and in the number of phasic REMs following learning tasks (Smith & Lapp, 1986; Smith & Rose, 1996).…”