Electrophysiological correlates of behavioural changes in vigilance in vegetative state and minimally conscious state

Abstract

The existence of normal sleep in patients in a vegetative state is still a matter of debate. Previous electrophysiological sleep studies in patients with disorders of consciousness did not differentiate patients in a vegetative state from patients in a minimally conscious state. Using high-density electroencephalographic sleep recordings, 11 patients with disorders of consciousness (six in a minimally conscious state, five in a vegetative state) were studied to correlate the electrophysiological changes associated with sleep to behavioural changes in vigilance (sustained eye closure and muscle inactivity). All minimally conscious patients showed clear electroencephalographic changes associated with decreases in behavioural vigilance. In the five minimally conscious patients showing sustained behavioural sleep periods, we identified several electrophysiological characteristics typical of normal sleep. In particular, all minimally conscious patients showed an alternating non-rapid eye movement/rapid eye movement sleep pattern and a homoeostatic decline of electroencephalographic slow wave activity through the night. In contrast, for most patients in a vegetative state, while preserved behavioural sleep was observed, the electroencephalographic patterns remained virtually unchanged during periods with the eyes closed compared to periods of behavioural wakefulness (eyes open and muscle activity). No slow wave sleep or rapid eye movement sleep stages could be identified and no homoeostatic regulation of sleep-related slow wave activity was observed over the night-time period. In conclusion, we observed behavioural, but no electrophysiological, sleep wake patterns in patients in a vegetative state, while there were near-to-normal patterns of sleep in patients in a minimally conscious state. These results shed light on the relationship between sleep electrophysiology and the level of consciousness in severely brain-damaged patients. We suggest that the study of sleep and homoeostatic regulation of slow wave activity may provide a complementary tool for the assessment of brain function in minimally conscious state and vegetative state patients.

Figure 1

Sleep in six patients in a minimally conscious state. Left: electrooculogram, EEG and EMG 10 s traces for three states: Wake, slow-wave sleep and REM sleep. One subject, MCS6, did not have any REM during the recording. Right: Topographic distribution of slow wave activity during non-rapid eye movement (NREM) sleep for the entire night. Colour bars represent the average absolute electrographic power (uV2/0.25 Hz frequency bin for the 0.5–4.5 Hz range) expressed as the maximum and minimum power for each individual.

Figure 2

Homoeostatic decline in slow wave activity of five patients in a minimally conscious state. Hypnogram and slow-wave activity time course. Sleep stages represented as REM, Wake, Stages 1, 2 and 3. The time course of slow-wave activity for a single channel near Fz is expressed as a percentage of the mean slow-wave activity reading for the entire night. MCS = patients in a minimally conscious state.

Figure 3

Behavioral sleep patterns for patients in a vegetative state and slow-wave activity topography. (Left) electrooculogram, EEG and EMG 10 s traces for eyes open and eyes closed. (Right) Topographic distribution of the average slow wave activity during the eyes closed condition for the entire night. Colour bars represent the absolute electrographic power (uV2/0.25 Hz frequency bin for the 0.5–4.5 Hz range) expressed as the maximum and minimum power for each individual. SWA = slow-wave activity; VS = patients in a vegetative state.

Figure 4

Hypnogram and slow-wave activity time course in four patients in a vegetative state. Behavioural sleep patterns represented as eyes open and eyes closed. The time course of slow-wave activity for a single channel near Fz is expressed as a percentage of the mean slow-wave activity reading for the entire night.