Cortical Function in Acute Severe Traumatic Brain Injury and at Recovery: A Longitudinal fMRI Case Study

Abstract

Differences in the functional integrity of the brain from acute severe brain injury to subsequent recovery of consciousness have not been well documented. Functional magnetic resonance imaging (fMRI) may elucidate this issue as it allows for the objective measurement of brain function both at rest and in response to stimuli. Here, we report the cortical function of a patient with a severe traumatic brain injury (TBI) in a critically ill state and at subsequent functional recovery 9-months post injury. A series of fMRI paradigms were employed to assess sound and speech perception, command following, and resting state connectivity. The patient retained sound perception and speech perception acutely, as indexed by his fMRI responses. Command following was absent acutely, but was present at recovery. Increases in functional connectivity across multiple resting state networks were observed at recovery. We demonstrate the clinical utility of fMRI in assessing cortical function in a patient with severe TBI. We suggest that hallmarks of the recovery of consciousness are associated with neural activity to higher-order cognitive tasks and increased resting state connectivity.

Keywords: awareness; coma; consciousness; disorders of consciousness; traumatic brain injury.

Figure 1

Structural imaging of the reported patient. (A) CT imaging showed preserved grey and white matter differentiation with no major mass lesion or mass effect. A small left subcortical frontal hemorrhage was seen and associated with diffuse axonal injury. (B) Susceptibility weighted imaging showed punctate foci of parenchymal susceptibility (indicated by the circles) in both cerebral hemispheres, consistent with diffuse axonal injury *. (C) Susceptibility weighted imaging revealed a unilateral right sided midbrain injury. There were punctate foci of parenchymal susceptibility from blood in the right cerebral peduncle, as indicated by the white arrow *. (D) Susceptibility weighted imaging showed punctate foci of parenchymal susceptibility from blood in the left subcortical frontal lobe, as indicated by the white arrow *. * Black shaded areas are a result of motion artifact.

Figure 2

Schematic timeline of the patient from acute care admission to the follow-up fMRI scan. Written, informed consent was obtained from the patient′s substitute decision-maker for the first fMRI scan and subsequently, from the patient once consciousness and capacity were regained.

Figure 3

Auditory perception acutely and at recovery. (A) Neural responses to the auditory perception paradigm in acute brain injury *. (B) Neural responses to the auditory perception paradigm 9-months post-injury *. (C) The patterns of activity in the auditory perception paradigm corresponding to the peak voxel co-ordinates in each contrast. The acute scan and recovery scan parameters are plotted adjacent to the mean activity of 14 healthy participants [13]. The error bars indicate the standard deviation of the healthy controls. * Individual patient results are thresholded at p < 0.05, FWE corrected for multiple comparisons.

Figure 4

Neural responses to the auditory perception paradigm when comparing differences in activity between the recovery and acute scan (Recovery > Acute). Individual patient results are thresholded at p < 0.05, FWE corrected for multiple comparisons.

Figure 5

(A) Neural responses to the spatial navigation paradigm when comparing the activity of the recovery to the acute scan. Individual patient results are thresholded at p < 0.001. Images are masked inclusively by the group analysis of healthy control participants. (B) The difference in activity in the left parahippocampal gyrus is plotted adjacent to the mean activity observed in this region in 14 healthy participants performing the same task [20]. The error bars indicate the standard deviation of the healthy controls.

Figure 6

Resting state connectivity acutely and at recovery. (A) A significant increase in correlation to the spatial template averaged across 10 resting state networks were observed at recovery. The * denotes a significant difference in correlation between the two time points. (B) Increases by at least two-fold in connectivity were observed in the visual medial, default mode, sensorimotor, and auditory networks at recovery.