Conscious processing of narrative stimuli synchronizes heart rate between individuals.

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 synchronize between subjects by presenting an identical narrative stimulus. As predicted, we find significant inter-subject correlation of heart rate (ISC-HR) when subjects are presented with an auditory or audiovisual narrative. Consistent with our hypothesis, we find that ISC-HR is reduced when subjects are distracted from the narrative, and higher ISC-HR predicts better recall of the narrative. Finally, patients with disorders of consciousness have lower ISC-HR, as compared to healthy individuals. 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.

The prognostic value of resting-state EEG in acute post-traumatic unresponsive states.

Accurate early prognostication is vital for appropriate long-term care decisions after traumatic brain injury. While measures of resting-state EEG oscillations and their network properties, derived from graph theory, have been shown to provide clinically useful information regarding diagnosis and recovery in patients with chronic disorders of consciousness, little is known about the value of these network measures when calculated from a standard clinical low-density EEG in the acute phase post-injury. To investigate this link, we first validated a set of measures of oscillatory network features between high-density and low-density resting-state EEG in healthy individuals, thus ensuring accurate estimation of underlying cortical function in clinical recordings from patients. Next, we investigated the relationship between these features and the clinical picture and outcome of a group of 18 patients in acute post-traumatic unresponsive states who were not following commands 2 days+ after sedation hold. While the complexity of the alpha network, as indexed by the standard deviation of the participation coefficients, was significantly related to the patients' clinical picture at the time of EEG, no network features were significantly related to outcome at 3 or 6 months post-injury. Rather, mean relative alpha power across all electrodes improved the accuracy of outcome prediction at 3 months relative to clinical features alone. These results highlight the link between the alpha rhythm and clinical signs of consciousness and suggest the potential for simple measures of resting-state EEG band power to provide a coarse snapshot of brain health for stratification of patients for rehabilitation, therapy and assessments of both covert and overt cognition.

Covert Speech Comprehension Predicts Recovery From Acute Unresponsive States.

OBJECTIVE: Patients with traumatic brain injury who fail to obey commands after sedation-washout pose one of the most significant challenges for neurological prognostication. Reducing prognostic uncertainty will lead to more appropriate care decisions and ensure provision of limited rehabilitation resources to those most likely to benefit. Bedside markers of covert residual cognition, including speech comprehension, may reduce this uncertainty. METHODS: We recruited 28 patients with acute traumatic brain injury who were 2 to 7 days sedation-free and failed to obey commands. Patients heard streams of isochronous monosyllabic words that built meaningful phrases and sentences while their brain activity via electroencephalography (EEG) was recorded. In healthy individuals, EEG activity only synchronizes with the rhythm of phrases and sentences when listeners consciously comprehend the speech. This approach therefore provides a measure of residual speech comprehension in unresponsive patients. RESULTS: Seventeen and 16 patients were available for assessment with the Glasgow Outcome Scale Extended (GOSE) at 3 months and 6 months, respectively. Outcome significantly correlated with the strength of patients' acute cortical tracking of phrases and sentences (r > 0.6, p < 0.007), quantified by inter-trial phase coherence. Linear regressions revealed that the strength of this comprehension response (beta = 0.603, p = 0.006) significantly improved the accuracy of prognoses relative to clinical characteristics alone (eg, Glasgow Coma Scale [GCS], computed tomography [CT] grade). INTERPRETATION: A simple, passive, auditory EEG protocol improves prognostic accuracy in a critical period of clinical decision making. Unlike other approaches to probing covert cognition for prognostication, this approach is entirely passive and therefore less susceptible to cognitive deficits, increasing the number of patients who may benefit. ANN NEUROL 2021;89:646-656.

Event-related potentials reflect prediction errors and pop-out during comprehension of degraded speech.

Comprehension of degraded speech requires higher-order expectations informed by prior knowledge. Accurate top-down expectations of incoming degraded speech cause a subjective semantic 'pop-out' or conscious breakthrough experience. Indeed, the same stimulus can be perceived as meaningless when no expectations are made in advance. We investigated the event-related potential (ERP) correlates of these top-down expectations, their error signals and the subjective pop-out experience in healthy participants. We manipulated expectations in a word-pair priming degraded (noise-vocoded) speech task and investigated the role of top-down expectation with a between-groups attention manipulation. Consistent with the role of expectations in comprehension, repetition priming significantly enhanced perceptual intelligibility of the noise-vocoded degraded targets for attentive participants. An early ERP was larger for mismatched (i.e. unexpected) targets than matched targets, indicative of an initial error signal not reliant on top-down expectations. Subsequently, a P3a-like ERP was larger to matched targets than mismatched targets only for attending participants-i.e. a pop-out effect-while a later ERP was larger for mismatched targets and did not significantly interact with attention. Rather than relying on complex post hoc interactions between prediction error and precision to explain this apredictive pattern, we consider our data to be consistent with prediction error minimization accounts for early stages of processing followed by Global Neuronal Workspace-like breakthrough and processing in service of task goals.

Skipping a Beat: Heartbeat-Evoked Potentials Reflect Predictions during Interoceptive-Exteroceptive Integration.

Several theories propose that emotions and self-awareness arise from the integration of internal and external signals and their respective precision-weighted expectations. Supporting these mechanisms, research indicates that the brain uses temporal cues from cardiac signals to predict auditory stimuli and that these predictions and their prediction errors can be observed in the scalp heartbeat-evoked potential (HEP). We investigated the effect of precision modulations on these cross-modal predictive mechanisms, via attention and interoceptive ability. We presented auditory sequences at short (perceived synchronous) or long (perceived asynchronous) cardio-audio delays, with half of the trials including an omission. Participants attended to the cardio-audio synchronicity of the tones (internal attention) or the auditory stimuli alone (external attention). Comparing HEPs during omissions allowed for the observation of pure predictive signals, without contaminating auditory input. We observed an early effect of cardio-audio delay, reflecting a difference in heartbeat-driven expectations. We also observed a larger positivity to the omissions of sounds perceived as synchronous than to the omissions of sounds perceived as asynchronous when attending internally only, consistent with the role of attentional precision for enhancing predictions. These results provide support for attentionally modulated cross-modal predictive coding and suggest a potential tool for investigating its role in emotion and self-awareness.