Decoding Mental States after Severe Brain Injury

Some patients with disorders of consciousness retain sensory and cognitive abilities that are not apparent from their outward behaviour. It is crucial to identify and characterise these covert abilities for diagnosis, prognosis, and medical ethics. This thesis uses neuroimaging techniques to investigate cognitive preservation and awareness in patients who are behaviourally non-responsive due to acquired brain injuries. In the first chapter, a large sample of healthy volunteers, including experienced athletes and musicians, imagined actions of varying complexity and familiarity. Motor imagery involving certain complex, familiar actions correlated with a more robust sensorimotor rhythm. In the second chapter, several patients with disorders of consciousness participated in multiple experiments based on neural responses to mental imagery, including one task featuring complex, familiar imagined actions. Although the patients did not generate enhanced sensorimotor rhythms for the complex, familiar motor imagery, the detection of covert cognition was more sensitive owing to the multi-modal nature of the assessment. In the final empirical chapter, a sample of healthy volunteers and a heterogeneous cohort of patients with disorders of consciousness completed a novel oddball task based on tactile stimulation. Critically, this task delineated an attentional hierarchy in the patient sample, and patients with the ability to follow commands were differentiated from those unable to do so by event-related potential evidence of attentional orienting. Due to the heterogeneity of aetiology and pathology in the disorders of consciousness, these patients vary in their suitability for neuroimaging, the preservation of neural structures, and the cognitive resources available to them. Assessments of several perceptual and cognitive abilities supported by spatially-distinct brain regions and indexed by multiple neural signatures are therefore required to accurately characterise a patient’s abilities and probable subjective experience

Progression from Vegetative to Minimally Conscious State Is Associated with Changes in Brain Neural Response to Passive Tasks: A Longitudinal Single-Case Functional MRI Study

Objectives: Functional magnetic resonance imaging (fMRI) may be adopted as a complementary tool for bedside observation in the disorders of consciousness (DOC). However, the diagnostic value of this technique is still debated because of the lack of accuracy in determining levels of consciousness within a single patient. Recently, Giacino and colleagues (2014) hypothesized that a longitudinal fMRI evaluation may provide a more informative assessment in the detection of residual awareness. The aim of this study was to measure the correspondence between clinically defined level of awareness and neural responses within a single DOC patient. Methods: We used a follow-up fMRI design in combination with a passive speech-processing task. Patient\u27s consciousness was measured through time by using the Coma Recovery Scale. Results: The patient progressed from a vegetative state (VS) to a minimally conscious state (MCS). Patient\u27s task-related neural responses mirrored the clinical change from a VS to an MCS. Specifically, while in an MCS, but not a VS, the patient showed a selective recruitment of the left angular gyrus when he listened to a native speech narrative, as compared to the reverse presentation of the same stimulus. Furthermore, the patient showed an increased response in the language-related brain network and a greater deactivation in the default mode network following his progression to an MCS. Conclusions: Our findings indicate that longitudinal assessment of brain responses to passive stimuli can contribute to the definition of the clinical status in individual patients with DOC and represents an adequate counterpart of the bedside assessment during the diagnostic decision-making process. (JINS, 2016, 22, 620-630

A hierarchy of event-related potential markers of auditory processing in disorders of consciousness.

Functional neuroimaging of covert perceptual and cognitive processes can inform the diagnoses and prognoses of patients with disorders of consciousness, such as the vegetative and minimally conscious states (VS;MCS). Here we report an event-related potential (ERP) paradigm for detecting a hierarchy of auditory processes in a group of healthy individuals and patients with disorders of consciousness. Simple cortical responses to sounds were observed in all 16 patients; 7/16 (44%) patients exhibited markers of the differential processing of speech and noise; and 1 patient produced evidence of the semantic processing of speech (i.e. the N400 effect). In several patients, the level of auditory processing that was evident from ERPs was higher than the abilities that were evident from behavioural assessment, indicating a greater sensitivity of ERPs in some cases. However, there were no differences in auditory processing between VS and MCS patient groups, indicating a lack of diagnostic specificity for this paradigm. Reliably detecting semantic processing by means of the N400 effect in passively listening single-subjects is a challenge. Multiple assessment methods are needed in order to fully characterise the abilities of patients with disorders of consciousness

Multiple tasks and neuroimaging modalities increase the likelihood of detecting covert awareness in patients with disorders of consciousness

Minimal or inconsistent behavioural responses to command make it challenging to accurately diagnose the level of awareness of a patient with a Disorder of Consciousness (DOC). By identifying markers of mental imagery being covertly performed to command, functional neuroimaging (fMRI, EEG) has shown that some of these patients are aware despite their lack of behavioural responsiveness. We report the findings of behavioural, fMRI, and EEG approaches to detecting command-following in a group of patients with DOC. From an initial sample of 14 patients, complete data across all tasks was obtained in six cases. Behavioural evaluations were performed with the Coma Recovery Scale - Revised. Both fMRI and EEG evaluations involved the completion of previously validated mental imagery tasks - i.e., motor imagery (EEG and fMRI) and spatial navigation imagery (fMRI). One patient exhibited statistically significant evidence of motor imagery in both the fMRI and EEG tasks, despite being unable to follow commands behaviourally. Two behaviourally non-responsive patients produced appropriate activation during the spatial navigation fMRI task. However, neither of these patients successfully completed the motor imagery tasks, likely due to specific motor area damage in at least one of these cases. A further patient demonstrated command following only in the EEG motor imagery task, and two patients did not demonstrate command following in any of the behavioural, EEG, or fMRI assessments. Due to the heterogeneity of aetiology and pathology in this group, DOC patients vary in terms of their suitability for some forms of neuroimaging, the preservation of specific neural structures, and the cognitive resources that may be available to them. Assessments of a range of cognitive abilities supported by spatially-distinct brain regions and indexed by multiple neural signatures are therefore required in order to accurately characterise a patient’s level of residual cognition and awareness

24-h polysomnographic recordings and electrophysiological spectral analyses from a cohort of patients with chronic disorders of consciousness

Fourteen patients with severe brain injuries and chronic disorders of consciousness underwent polysomnographic recordings for a 24-h period. Their electrophysiological data were scored using a modified sleep staging system employed in a previous study of similar patients (J Head Trauma Rehabil 30:334–346, 2015). In addition to sleep scoring, the patients’ data were compared with a sample of approximately age-matched healthy volunteers in the spectral domain. All patients demonstrated some form of a sleep–wake cycle; however, the integrity of normal sleep features was remarkably heterogenous across individuals, and in some cases, sleep was significantly impoverished. In three patients, these cycles were biphasic and comprised of only alternating periods of wakefulness and sleep-like electrophysiological activity. Two patients demonstrated a sleep–wake cycle that included all sleep stages aside from non-REM stage 3, and another two patients demonstrated a sleep–wake cycle that included all sleep stages aside from REM sleep. The remaining seven patients, which included patients diagnosed as being in a minimally conscious state and patients diagnosed as being in a vegetative state (unresponsive wakefulness syndrome), demonstrated full sleep architecture, including k-complexes, REMs, and slow wave sleep. However, three of the patients with full sleep architecture did not generate sleep spindles. Altogether, these findings highlight the heterogeneity of brain function among patients with disorders of consciousness, regardless of their diagnostic category. Polysomnography is a useful tool to complement other behavioural and physiological assessments that characterize the abilities of each patient

Complexity and familiarity enhance single-trial detectability of imagined movements with electroencephalography

Objective We sought to determine whether the sensorimotor rhythms (SMR) elicited during motor imagery (MI) of complex and familiar actions could be more reliably detected with electroencephalography (EEG), and subsequently classified on a single-trial basis, than those elicited during relatively simpler imagined actions. Methods Groups of healthy volunteers, including experienced pianists and ice hockey players, performed MI of varying complexity and familiarity. Their electroencephalograms were recorded and compared using brain-computer interface (BCI) approaches and spectral analyses. Results Relative to simple MI, significantly more participants produced classifiable SMR for complex MI. During MI of performance of a complex musical piece, the EEG of the experienced pianists was classified significantly more accurately than during MI of performance of a simpler musical piece. The accuracy of EEG classification was also significantly more sustained during complex MI. Conclusion MI of complex actions results in EEG responses that are more reliably classified for more individuals than MI of relatively simpler actions, and familiarity with actions enhances these responses in some cases. Significance The accuracy of SMR-based BCIs in non-communicative patients may be improved by employing familiar and complex actions. Increased sensitivity to MI may also improve diagnostic accuracy for severely brain-injured patients in a vegetative state