Highlights d Narrative stimuli can synchronize fluctuations of heart rate between individuals d This interpersonal synchronization is modulated by attention and predicts memory d These effects on heart rate cannot be explained by modulation of respiratory patterns d Synchrony is lower in patients with disorders of consciousness

Our work shows a link between residual cognitive processing and the modulation of autonomic somatic markers. These results open a new window to evaluate patients with disorders of consciousness via the embodied paradigm, according to which body-brain functions contribute to a holistic approach to conscious processing. Ann Neurol 2017;82:578-591.

Early accurate clinical diagnosis of VS/UWS or MCS conveys a strong prognostic value of survival and of consciousness recovery.

Pupil dilation has been reliably identified as a physiological marker of consciously reportable mental effort. This classical finding raises the question of whether or not pupil dilation could be a specific somatic signature of conscious processing. In order to explore this possibility, we engaged healthy volunteers in the ‘local global’ auditory paradigm we previously designed to disentangle conscious from non-conscious processing of novelty. We discovered that consciously reported violations of global (inter-trials) regularity were associated with a pupil dilation effect both in an active counting task and in a passive attentive task. This pupil dilation effect was detectable both at the group-level and at the individual level. In contrast, unreported violations of this global regularity, as well as unreported violations of local (intra-trial) regularity that do not require conscious access, were not associated with a pupil dilation effect. We replicated these findings in a phonemic version of the ‘local global’. Taken together these results strongly suggest that pupil dilation is a somatic marker of conscious access in the auditory modality, and that it could therefore be used to easily probe conscious processing at the individual level without interfering with participant’s stream of consciousness by questioning him/her.

The use of cognitive evoked potentials in EEG is now part of the routine evaluation of non-communicating patients with disorders of consciousness in several specialized medical centers around the world. They typically focus on one or two cognitive markers, such as the mismatch negativity or the P3 to global auditory regularity. However it has become clear that none of these markers in isolation is at the same time sufficiently specific and sufficiently sensitive to be taken as the unique gold standard for diagnosing consciousness. A good way forward would be to combine several cognitive markers within the same test to improve evaluation. Furthermore, given the diversity of lesions leading to disorders of consciousness, it is important not only to probe whether a patient is conscious or not, but also to establish a more general and nuanced profile of the residual cognitive capacities of each patient using a combination of markers.In the present study we built a unique EEG protocol that probed 8 dimensions of cognitive processing in a single 1.5 h session. This protocol probed variants of classical markers together with new markers of spatial attention, which has not yet been studied in these patients. The eight dimensions were: (1) own name recognition, (2) temporal attention, (3) spatial attention, (4) detection of spatial incongruence (5) motor planning, and (6,7,8) modulations of these effects by the global context, reflecting higher-level functions. This protocol was tested in 15 healthy control subjects and in 17 patients with various etiologies, among which 13 could be included in the analysis. The results in the control group allowed a validation and a specific description of the cognitive levels probed by each marker. At the single-subject level, this combined protocol allowed assessing the presence of both classical and newly introduced markers for each patient and control, and revealed that the combination of several markers increased diagnostic sensitivity. The presence of a high-level effect in any of the three tested domains distinguished between minimally conscious and vegetative patients, while the presence of low-level effects was similar in both groups. In summary, this study constitutes a validated proof of concept in favor of probing multiple cognitive dimensions to improve the evaluation of non-communicating patients. At a more conceptual level, this EEG tool can help achieve a better understanding of disorders of consciousness by exploring consciousness in its multiple cognitive facets.

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Predicting the functional recovery of patients with severe neurological condition due to coronavirus disease 2019 (COVID-19) is a challenging task. Only limited outcome data are available, the pathophysiology is poorly understood, and the time-course of recovery is still largely unknown. Here, we report the case of a patient with COVID-19 associated encephalitis presenting as a prolonged state of unresponsiveness for two months, who finally fully recovered consciousness, functional communication, and autonomy after immunotherapy. In a multimodal approach, a high-density resting state EEG revealed a rich brain activity in spite of a severe clinical presentation. Using our previously validated algorithms, we could predict a possible improvement of consciousness in this patient. This case report illustrates the value of a multimodal approach capitalizing on advanced brain-imaging and bedside electrophysiology techniques to improve prognosis accuracy in this complex and new aetiology.

Heart rate has natural fluctuations that are typically ascribed to autonomic function. Recent evidence suggests that conscious processing can affect the timing of the heartbeat. We hypothesized that heart rate is modulated by conscious processing and therefore dependent on attentional focus. To test this we leverage the observation that neural processes can be synchronized between subjects by presenting an identical narrative stimulus. As predicted, we find significant inter-subject correlation of the heartbeat (ISC-HR) when subjects are presented with an auditory or audiovisual narrative. Consistent with the conscious processing hypothesis, we find that ISC-HR is reduced when subjects are distracted from the narrative, and that higher heart rate synchronization predicts better recall of the narrative. Finally, patients with disorders of consciousness who are listening to a story have lower ISC, as compared to healthy individuals, and that individual ISC-HR might predict a patients’ prognosis. We conclude that heart rate fluctuations are partially driven by conscious processing, depend on attentional state, and may represent a simple metric to assess conscious state in unresponsive patients.