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Evidence from recent electroencephalographic and magnetoencephalographic sleep studies is reviewed in relation to consciousness and dreams, two fundamental issues in psychoanalytic theory and practice. The rich dynamics of the macro- and microstructure of human sleep indicate specific brain disintegrating mechanisms as underlying the loss and alteration of consciousness in non-rapid eye movement (NREM) and REM sleep, respectively. Transient state changes and dynamic interactions between elements of sleep graphoelements (i.e. K-complexes and spindles) are described; these, beyond their involvement in controlling consciousness level, may support the consolidation or modification of therapeutic experiences. Higher powers than in awake-state gamma-band electrographic activity (known to underlie cognitive processes), which we observed in specific medial prefrontal cortical areas, are proposed to support content in dreaming (REM) and mentation (NREM). These areas lie in remarkably close proximity to the “default system” and “theory of mind” areas, which may be parts of the neural correlates of intrapsychic and intersubjective processes. Specific activations of limbic circuits were observed in REM sleep in consistency with the emotional content of dreams. Current brain imaging technology in sleep studies offers new opportunities to explore the mechanisms underlying consciousness and dreaming, a unique area of convergence between biology and psychology.