Neural coding of autonomic functions in different states of consciousness

Abstract

Detecting signs of residual neural activity in patients with altered states of consciousness is a crucial issue for the customization of neurorehabilitation treatments and clinical decision-making. With this large observational prospective study, we propose an innovative approach to detect residual signs of consciousness via the assessment of the amount of autonomic information coded within the brain. The latter was estimated by computing the mutual information (MI) between preprocessed EEG and ECG signals, to be then compared across consciousness groups, together with the absolute power and an international qualitative labeling. One-hundred seventy-four patients (73 females, 42%) were included in the study (median age of 65 years [IQR = 20], MCS +: 29, MCS -: 23, UWS: 29). Electroencephalography (EEG) information content was found to be mostly related to the coding of electrocardiography (ECG) activity, i.e., with higher MI (p < 0.05), in Unresponsive Wakefulness Syndrome and Minimally Consciousness State minus (MCS -). EEG-ECG MI, besides clearly discriminating patients in an MCS - and +, significantly differed between lesioned areas (sides) in a subgroup of unilateral hemorrhagic patients. Crucially, such an accessible and non-invasive measure of residual consciousness signs was robust across electrodes and patient groups. Consequently, exiting from a strictly neuro-centric consciousness detection approach may be the key to provide complementary insights for the objective assessment of patients' consciousness levels and for the patient-specific planning of rehabilitative interventions.

Keywords: Brain–heart interaction; Disorders of consciousness; EEG-ECG mutual information; Minimally Consciousness State; Quantitative Correlates of Consciousness.

Fig. 1

EEG Power Spectral Density across consciousness states. Absolute power is reported on the scalp for each consciousness state (columns) and each frequency band (rows). The topographic map is obtained by performing a spatial 2D interpolation of the PSD values at each electrode (median across patients of that group)

Fig. 2

EEG-ECG Mutual Information across consciousness states. Spatial interpolation of median (across patients) MI values for each consciousness group (upper subplots). Box-plots with electrode-wise groups comparisons of MI across consciousness states (lower subplots) with related pair-wise Dunn-Bonferroni significances (conditioned to Kruskal–Wallis significance). Subplots are distributed in space following approximate position within the 10–20 system

Fig. 3

EEG-ECG Mutual Information across hemorrhagic sites. Spatial interpolation of median (across only hemorrhagic patients) MI values for higher and lower consciousness levels (left versus right) and for each lesion side (top versus bottom)