Brain processing of stimulus deviance during slow-wave and paradoxical sleep: a study of human auditory evoked responses using the oddball paradigm

Abstract

Auditory evoked potentials (AEPs) to frequent (90%) and deviant (10%) tones were recorded during both wakefulness and all-night sleep in eight drug-free volunteers. During presleep waking (10:00-11:00 p.m.), deviant stimuli elicited, in all subjects, a prominent "P300" wave of parieto-central topography, culminating at 344 ms (average), which was absent in response to frequent tones. This "presleep P300" was delayed and reduced relative to values obtained during full wakefulness (3:00-7:00 p.m.) in a control group. Passage from waking to sleep stage I was characterized by a progressive attenuation and delay of the P300 wave in response to deviant stimuli, without major changes in AEP morphology as compared to the waking state. Thus, in terms of cognitive evoked potentials (EPs), sleep stage I appeared more as a "weak" state of wakefulness than a true phase of sleep. During sleep stages II, III, and IV, both frequent and deviant tones evoked AEPs that closely resembled K-complexes. Responses to rare stimuli were four-to-five times larger than those to frequent tones, this likely being the result of K-complex habituation to monotonous stimuli. During paradoxical sleep (PS), AEP morphology again became comparable to that of wakefulness. Notably, a "P3" wave with similar topography as the waking P300 appeared in response to deviant stimuli exclusively. Thus, even though the brain seems able to detect stimulus deviance during all sleep stages, only during stage I and PS were the electrophysiological counterparts of deviance detection comparable to those of the waking state. Our results support the view that PS is not a state of "sensory isolation"; failure to respond to external stimuli during this stage may depend upon mechanisms occurring only after the sensory input has undergone cognitive analysis.