Somatosensory attention identifies both overt and covert awareness in disorders of consciousness

Objective Some patients diagnosed with disorders of consciousness retain sensory and cognitive abilities beyond those apparent from their overt behavior. Characterizing these covert abilities is crucial for diagnosis, prognosis, and medical ethics. This multimodal study investigates the relationship between electroencephalographic evidence for perceptual/cognitive preservation and both overt and covert markers of awareness. Methods Fourteen patients with severe brain injuries were evaluated with an electroencephalographic vibrotactile attention task designed to identify a hierarchy of residual somatosensory and cognitive abilities: (1) somatosensory steady-state evoked responses, (2) bottom-up attention orienting (P3a event-related potential), and (3) top-down attention (P3b event-related potential). Each patient was also assessed with a clinical behavioral scale and 2 functional magnetic resonance imaging assessments of covert command following. Results Six patients produced only sensory responses, with no evidence of cognitive event-related potentials. A further 8 patients demonstrated reliable bottom-up attention-orienting responses (P3a). No patient showed evidence of top-down attention (P3b). Only those patients who followed commands, whether overtly with behavior or covertly with functional neuroimaging, also demonstrated event-related potential evidence of attentional orienting. Interpretation Somatosensory attention-orienting event-related potentials differentiated patients who could follow commands from those who could not. Crucially, this differentiation was irrespective of whether command following was evident through overt external behavior, or through covert functional neuroimaging methods. Bedside electroencephalographic methods may corroborate more expensive and challenging methods such as functional neuroimaging, and thereby assist in the accurate diagnosis of awareness

Utilizing Visual Attention and Inclination to Facilitate Brain-Computer Interface Design in an Amyotrophic Lateral Sclerosis Sample

Individuals who suffer from amyotrophic lateral sclerosis (ALS) have a loss of motor control and possibly the loss of speech. A brain-computer interface (BCI) provides a means for communication through nonmuscular control. Visual BCIs have shown the highest potential when compared to other modalities; nonetheless, visual attention concepts are largely ignored during the development of BCI paradigms. Additionally, individual performance differences and personal preference are not considered in paradigm development. The traditional method to discover the best paradigm for the individual user is trial and error. Visual attention research and personal preference provide the building blocks and guidelines to develop a successful paradigm. This study is an examination of a BCI-based visual attention assessment in an ALS sample. This assessment takes into account the individual’s visual attention characteristics, performance, and personal preference to select a paradigm. The resulting paradigm is optimized to the individual and then tested online against the traditional row-column paradigm. The optimal paradigm had superior performance and preference scores over row-column. These results show that the BCI needs to be calibrated to individual differences in order to obtain the best paradigm for an end user

Sensorimotor Modulations by Cognitive Processes During Accurate Speech Discrimination: An EEG Investigation of Dorsal Stream Processing

Internal models mediate the transmission of information between anterior and posterior regions of the dorsal stream in support of speech perception, though it remains unclear how this mechanism responds to cognitive processes in service of task demands. The purpose of the current study was to identify the influences of attention and working memory on sensorimotor activity across the dorsal stream during speech discrimination, with set size and signal clarity employed to modulate stimulus predictability and the time course of increased task demands, respectively. Independent Component Analysis of 64–channel EEG data identified bilateral sensorimotor mu and auditory alpha components from a cohort of 42 participants, indexing activity from anterior (mu) and posterior (auditory) aspects of the dorsal stream. Time frequency (ERSP) analysis evaluated task-related changes in focal activation patterns with phase coherence measures employed to track patterns of information flow across the dorsal stream. ERSP decomposition of mu clusters revealed event-related desynchronization (ERD) in beta and alpha bands, which were interpreted as evidence of forward (beta) and inverse (alpha) internal modeling across the time course of perception events. Stronger pre-stimulus mu alpha ERD in small set discrimination tasks was interpreted as more efficient attentional allocation due to the reduced sensory search space enabled by predictable stimuli. Mu-alpha and mu-beta ERD in peri- and post-stimulus periods were interpreted within the framework of Analysis by Synthesis as evidence of working memory activity for stimulus processing and maintenance, with weaker activity in degraded conditions suggesting that covert rehearsal mechanisms are sensitive to the quality of the stimulus being retained in working memory. Similar ERSP patterns across conditions despite the differences in stimulus predictability and clarity, suggest that subjects may have adapted to tasks. In light of this, future studies of sensorimotor processing should consider the ecological validity of the tasks employed, as well as the larger cognitive environment in which tasks are performed. The absence of interpretable patterns of mu-auditory coherence modulation across the time course of speech discrimination highlights the need for more sensitive analyses to probe dorsal stream connectivity

A brain-machine interface for assistive robotic control

Brain-machine interfaces (BMIs) are the only currently viable means of communication for many individuals suffering from locked-in syndrome (LIS) – profound paralysis that results in severely limited or total loss of voluntary motor control. By inferring user intent from task-modulated neurological signals and then translating those intentions into actions, BMIs can enable LIS patients increased autonomy. Significant effort has been devoted to developing BMIs over the last three decades, but only recently have the combined advances in hardware, software, and methodology provided a setting to realize the translation of this research from the lab into practical, real-world applications. Non-invasive methods, such as those based on the electroencephalogram (EEG), offer the only feasible solution for practical use at the moment, but suffer from limited communication rates and susceptibility to environmental noise. Maximization of the efficacy of each decoded intention, therefore, is critical. This thesis addresses the challenge of implementing a BMI intended for practical use with a focus on an autonomous assistive robot application. First an adaptive EEG- based BMI strategy is developed that relies upon code-modulated visual evoked potentials (c-VEPs) to infer user intent. As voluntary gaze control is typically not available to LIS patients, c-VEP decoding methods under both gaze-dependent and gaze- independent scenarios are explored. Adaptive decoding strategies in both offline and online task conditions are evaluated, and a novel approach to assess ongoing online BMI performance is introduced. Next, an adaptive neural network-based system for assistive robot control is presented that employs exploratory learning to achieve the coordinated motor planning needed to navigate toward, reach for, and grasp distant objects. Exploratory learning, or “learning by doing,” is an unsupervised method in which the robot is able to build an internal model for motor planning and coordination based on real-time sensory inputs received during exploration. Finally, a software platform intended for practical BMI application use is developed and evaluated. Using online c-VEP methods, users control a simple 2D cursor control game, a basic augmentative and alternative communication tool, and an assistive robot, both manually and via high-level goal-oriented commands

Effects of hand orientation on motor imagery - event related potentials suggest kinesthetic motor imagery to solve the hand laterality judgment task

Motor imagery (MI) refers to the process of imagining the execution of a specific motor action without actually producing an overt movement. Two forms of MI have been distinguished: visual MI and kinesthetic MI. To distinguish between these forms of MI we employed an event related potential (ERP) study to measure interference effects induced by hand orientation manipulations in a hand laterality judgement task. We hypothesized that this manipulation should only affect kinesthetic MI but not visual MI. The ERPs elicited by rotated hand stimuli contained the classic rotation related negativity (RRN) with respect to palm view stimuli. We observed that laterally rotated stimuli led to a more marked RRN than medially rotated stimuli. This RRN effect was observed when participants had their hands positioned in either a straight (control) or an inward rotated posture, but not when their hands were positioned in an outward rotated posture. Posture effects on the ERP-RRN have not previously been studied. Apparently, a congruent hand posture (hands positioned in an outward rotated fashion) facilitates the judgement of the otherwise more demanding laterally rotated hand stimuli. These ERP findings support a kinesthetic interpretation of MI involved in solving the hand laterality judgement task. The RRN may be used as a non-invasive marker for kinesthetic MI and seems useful in revealing the covert behavior of MI in e.g. rehabilitation programs

An fMRI Study of Command Following and Communication Using Overt and Covert Motor Responses: Implications for Disorders of Consciousness

We used functional magnetic resonance imaging (fMRI) to explore neural mechanisms of command following or communicating using executed or imagined movements, in order to understand why most covertly aware patients cannot communicate. 15 healthy participants executed or imagined arm movements that were either selected by them or pre-determined. We also explored non-volitional motor activity by passively moving participants. Response selection involved greater activity in high-level associative areas in frontal and parietal regions than following commands. Furthermore, there was no interaction between response and modality. Neural activity during passive movement exceeded that of active (volitional) movement in sensorimotor regions. Our results suggest that the ability to select between motor responses is not dependent on how that response is expressed (via motor execution/imagery). They also suggest a potential neural basis of the distinction in cognitive abilities seen in DOCs. Finally, passive movement could be applied to study unresponsive patients’ motor systems

Face recognition deficits in a patient with Alzheimer's Disease: amnesia or agnosia? The importance of electrophysiological markers for differential diagnosis

Face recognition deficits are frequently reported in Alzheimer's disease (AD) and often attributed to memory impairment. However, it has been hypothesized that failure in identifying familiar people could also be due to deficits in higher-level perceptual processes, since there is evidence showing a reduced inversion effect for faces but not for cars in AD. To address the involvement of these higher processes, we investigated event-related potential (ERP) neural correlates of faces in a patient with AD showing a face recognition deficit. Eight healthy participants were tested as a control group. Participants performed different tasks following the stimulus presentation. In experiment 1, they should indicate whether the stimulus was either a face or a house or a scrambled image. In experiments 2 and 3, they should discriminate between upright and inverted faces (in experiment 2, stimuli were faces with neutral or fearful expressions, while in experiment 3, stimuli were famous or unfamiliar faces). Electrophysiological results reveal that the typical face-specific modulation of the N170 component, which is thought to reflect the structural encoding of faces, was not present in patient MCG, despite being affected by the emotional content of the face implicitly processed by MCG. Conversely, the N400 component, which is thought to reflect the recruitment of the memory trace of the face identity, was found to be implicitly modulated in MCG. These results may identify a possible role for gnosic processes in face recognition deficits in AD and suggest the importance of adopting an integrated approach to the AD diagnosis while considering electrophysiological markers

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