Abstract
It is well established that some patients, who are deemed to have disorders of consciousness, remain entirely behaviorally non-responsive and are diagnosed as being in a vegetative state, yet can nevertheless demonstrate covert awareness of their external environment by modulating their brain activity, a phenomenon known as cognitive-motor dissociation. However, the extent to which these patients retain internal awareness remains unknown. To investigate the potential for internal and external awareness in patients with chronic disorders of consciousness (DoC), we asked whether the pattern of juxtaposition between the functional time-courses of the default mode (DMN) and fronto-parietal networks, shown in healthy individuals to mediate the naturally occurring dominance switching between internal and external aspects of consciousness, was present in these patients. We used a highly engaging movie by Alfred Hitchcock to drive the recruitment of the fronto-parietal networks, including the dorsal attention (DAN) and executive control (ECN) networks, and their maximal juxtaposition to the DMN in response to the complex stimulus, relative to rest and a scrambled, meaningless movie baseline condition. We tested a control group of healthy participants (N = 13/12) and two groups of patients with disorders of consciousness, one comprised of patients who demonstrated independent, neuroimaging-based evidence of covert external awareness (N = 8), and the other of those who did not (N = 8). Similarly to the healthy controls, only the group of patients with overt and, critically, covert external awareness showed significantly heightened differentiation between the DMN and the DAN in response to movie viewing relative to their resting state time-courses, which was driven by the movie's narrative. This result suggested the presence of functional integrity in the DMN and fronto-parietal networks and their relationship to one another in patients with covert external awareness. Similar to the effect in healthy controls, these networks became more strongly juxtaposed to one another in response to movie viewing relative to the baseline conditions, suggesting the potential for internal and external awareness during complex stimulus processing. Furthermore, our results suggest that naturalistic paradigms can dissociate between groups of DoC patients with and without covert awareness based on the functional integrity of brain networks.
Highlights
In the last decade, a population of patients has been identified who are demonstrably conscious, but entirely unable to speak or move willfully in any way, and remain behaviorally nonresponsive for several years [1,2,3,4,5,6,7,8]
During movie viewing the connectivity between the default mode network (DMN) and dorsal attention (DAN) [t(12) = 4.58, p < 0.001] and DMN and executive control (ECN) [t(12) = 4.03, p < 0.005] were significantly down-regulated during the movie relative to the resting state (Figure 3A)
As the measure of connectivity (Pearson correlation) reflected the degree of similarity between the networks’ functional time-courses, this result demonstrated that the functional response of each of the DAN/ECN became more dissimilar to that of the DMN during the movie relative to the resting state baseline
Summary
A population of patients has been identified who are demonstrably conscious, but entirely unable to speak or move willfully in any way, and remain behaviorally nonresponsive for several years [1,2,3,4,5,6,7,8]. Recent studies have shown that, despite the complete absence of external signs of awareness, a significant minority (∼14–19%) of patients thought to be in a VS are able to demonstrate conscious awareness by modulating their brain activity [2, 15] in different types of neuroimaging paradigms [e.g., [1, 3,4,5, 7, 8]], a phenomenon captured by the recentlycoined term “cognitive motor dissociation” (CMD) [16] Despite these advances, the mental life of behaviorally non-responsive patients— their capacity to have similar experiences as healthy individuals in response to everyday life events that involve both their awareness of oneself and awareness of one’s environment—had until recently remained largely unknown and inaccessible to empirical investigation. We tested whether DoC patients, who demonstrated independent covert external awareness, differently from patients who did not, showed a juxtaposition between the DMN and fronto-parietal functional time-courses that was strengthened by the complex stimulus
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