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. 2015 Apr 22;8:210-23.
doi: 10.1016/j.nicl.2015.04.011. eCollection 2015.

Filling in the Gaps: Anticipatory Control of Eye Movements in Chronic Mild Traumatic Brain Injury

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Free PMC article

Filling in the Gaps: Anticipatory Control of Eye Movements in Chronic Mild Traumatic Brain Injury

Mithun Diwakar et al. Neuroimage Clin. .
Free PMC article

Abstract

A barrier in the diagnosis of mild traumatic brain injury (mTBI) stems from the lack of measures that are adequately sensitive in detecting mild head injuries. MRI and CT are typically negative in mTBI patients with persistent symptoms of post-concussive syndrome (PCS), and characteristic difficulties in sustaining attention often go undetected on neuropsychological testing, which can be insensitive to momentary lapses in concentration. Conversely, visual tracking strongly depends on sustained attention over time and is impaired in chronic mTBI patients, especially when tracking an occluded target. This finding suggests deficient internal anticipatory control in mTBI, the neural underpinnings of which are poorly understood. The present study investigated the neuronal bases for deficient anticipatory control during visual tracking in 25 chronic mTBI patients with persistent PCS symptoms and 25 healthy control subjects. The task was performed while undergoing magnetoencephalography (MEG), which allowed us to examine whether neural dysfunction associated with anticipatory control deficits was due to altered alpha, beta, and/or gamma activity. Neuropsychological examinations characterized cognition in both groups. During MEG recordings, subjects tracked a predictably moving target that was either continuously visible or randomly occluded (gap condition). MEG source-imaging analyses tested for group differences in alpha, beta, and gamma frequency bands. The results showed executive functioning, information processing speed, and verbal memory deficits in the mTBI group. Visual tracking was impaired in the mTBI group only in the gap condition. Patients showed greater error than controls before and during target occlusion, and were slower to resynchronize with the target when it reappeared. Impaired tracking concurred with abnormal beta activity, which was suppressed in the parietal cortex, especially the right hemisphere, and enhanced in left caudate and frontal-temporal areas. Regional beta-amplitude demonstrated high classification accuracy (92%) compared to eye-tracking (65%) and neuropsychological variables (80%). These findings show that deficient internal anticipatory control in mTBI is associated with altered beta activity, which is remarkably sensitive given the heterogeneity of injuries.

Keywords: Anticipatory control; Attention; Magnetoencephalography; Mild traumatic brain injury; Visual tracking.

Figures

Fig. 1
Fig. 1
Illustration of the visual tracking task. Panel A illustrates the subject and screen positioning for viewing the visual tracking task. Panel B illustrates the target trajectory during the continuous tracking condition, where the target was visible throughout the period of tracking. Panel C illustrates an example of the target disappearing (outlined arrow and target) and then reappearing during the gap tracking condition.
Fig. 2
Fig. 2
Group differences in average radius (AR) and average phase (AP) error before, during, and after target occlusion. Graphs A and B display AR for the control and mTBI groups 208 ms before (Pre-Gap) and 208 ms during (within Gap) target occlusion. The mTBI patients showed significantly greater AR than the control group during both periods. Graphs C and D display AP for the control and mTBI groups 208 ms (Post-Gap 1) and 400 ms (Post-Gap 2) after the target reappeared. The mTBI group lagged behind the target during both post-gap periods (i.e., more negative values), whereas the control group tracked more closely to the target.
Fig. 3
Fig. 3
Phase error dynamics for 30° (A), 45° (B), and 60° (C) gap tracking conditions. Clusters of time points in blue survived multiple-comparisons, indicating significant differences in visual tracking between the control and mTBI groups. Clusters of time points in brown were significant uncorrected for multiple comparisons, but were not significant after correction for multiple-comparisons. White regions between the mTBI and control group time-courses failed to cluster and therefore, indicate no statistical difference between the groups. In the 30° and 45° gap conditions, the mTBI group exhibited significantly more phase lag than the control group after re-appearance of the target. Traces for periods between 250 ms before target disappearance and 500 ms after target reappearance are shown.
Fig. 4
Fig. 4
Regions showing group differences in MEG beta-band amplitude for the gap minus continuous condition comparison. Displayed regions are those that showed a significant group X tracking condition interaction. Numbers correspond to the regions that are detailed in Table 3. Images are display in radiological view. A) For regions 1 to 6, control subjects showed greater beta amplitude in the gap than the continuous condition, whereas the mTBI group showed lower beta amplitude in the gap than the continuous condition. B) For regions 7 to 10, the mTBI group showed greater beta amplitude in the gap than the continuous condition and control subjects showed lower beta amplitude in the gap than the continuous condition. C) Underlying gap minus continuous source activities for control subjects. D) Underlying gap minus continuous source activities for mTBI subjects. For panels C and D, hotter colors (red) indicate regions where gap tracking activity was greater than continuous tracking activity and cooler colors (blue) indicate regions where gap tracking activity was less than continuous tracking. ROIs from A and B are depicted in bright green and are overlaid onto activation in C and D.
Fig. 5
Fig. 5
Regional differences in MEG beta-amplitude between the gap minus continuous condition comparison. Significant differences between the control (brown bars) and mTBI (blue bars) groups were found for the gap minus continuous condition contrast in ten regions (see Table 3 and Fig. 3 for details). *Beta amplitude within a group for the gap minus continuous conditions contrast differed significantly from zero (p = 0.05). R and L = right and left hemispheres; B = bilateral; AG = angular gyrus; SMG = supramarginal gyrus; SPL = superior parietal lobule; Temp Pole = temporal pole; TPJ = temporal–parietal junction.
Fig. 6
Fig. 6
SVM classification accuracy of regional MEG beta-amplitude, visual tracking and neuropsychological measures. The graphs display the distance of each subject from the hyperplane that that best separated the two groups, which is a measure of the strength of classification. The graphs plot the classification weights (y axis) from the optimized SVM analysis for each subject in the control (brown circles) and mTBI groups (blue circles). Positively and negatively weighted values respectively designate whether subjects were classified into the control or mTBI group. The variables that contributed to the optimized SVM classification are listed in Table 4. A: Total classification accuracy using MEG beta-amplitude from 6 ROI was 92%. Two subjects in each group were incorrectly classified. B: Total classification accuracy using 3 visual tracking measures was 64%. Ten controls and 7 mTBI patients were incorrectly classified. C: Total classification accuracy using 8 neuropsychological measures was 80%. Four of the controls and 5 of the mTBI patients were incorrectly classified. D: Total classification accuracy using beta amplitude from 5 ROI and 3 neuropsychological measures was 94%. One control subject and 2 mTBI patients were incorrectly classified.
Fig. 7
Fig. 7
Scatter plots showing the relationship between average phase (AP) after the target reappeared and the expression of the optimized SVM function for MEG beta-amplitude in 6 ROI. The Post-Gap 1 and Post-Gap 2 periods were defined as 208 and 400 ms after the target reappeared, respectively. Negative and positive AP values (y axis) respectively signify lagging behind and tracking ahead of the target. Positively and negatively weighted values respectively designate whether subjects are more likely to classify into the control or mTBI group. Panels A and C: in the control group, more positive AP values during both post-gap periods (better anticipation of the target) were associated with higher SVM values (better neuronal functioning) (Post-Gap 1: rage = .39, p = .06; Post-Gap 2: rage = .41, p = .047). Panels B and D: in the mTBI group, no relationship was found between AP and SVM values.

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