The expression of trace conditioning during non-REM sleep and its relation to subjective experience

Research in animals has demonstrated that patterns of neural activity first seen during waking experience are later "replayed" during sleep, in hippocampal and cortical networks. The characteristics of memory reactivation during human sleep, however, have not yet been fully described. Meanwhile, the possible relationship of dreaming to this "replay" of memories in the sleeping brain is entirely unknown. In the present study, we induced hippocampus-dependent memory retrieval during human sleep using a "trace conditioning" procedure. Prior to sleep, subjects underwent either trace (hippocampus-dependent) or delay (hippocampus-independent) auditory fear conditioning. Conditioned stimuli were then presented to subjects during non-REM sleep. Both delay-conditioned and trace-conditioned subjects exhibited conditioned EEG responses during post-training sleep. However, selectively in trace-conditioned subjects, fear-conditioned cues also affected the valence of dreamed emotions. These findings suggest that hippocampus-dependent learning is accessible during non-REM sleep, and that hippocampus-mediated memory reactivation may be expressed, not only through neural activity in the sleeping brain, but also within concomitant subjective experience.