Magnetoencephalography Slow-Wave Detection in Patients with Mild Traumatic Brain Injury and Ongoing Symptoms Correlated with Long-Term Neuropsychological Outcome

Abstract

Mild traumatic brain injury (mTBI) is common in the United States, accounting for as many as 75-80% of all TBIs. It is recognized as a significant public health concern, but there are ongoing controversies regarding the etiology of persistent symptoms post-mTBI. This constellation of nonspecific symptoms is referred to as postconcussive syndrome (PCS). The present study combined results from magnetoencephalography (MEG) and cognitive assessment to examine group differences and relationships between brain activity and cognitive performance in 31 military and civilian individuals with a history of mTBI+PCS and 33 matched healthy control subjects. An operator-free analysis was used for MEG data to increase reliability of the technique. Subjects completed a comprehensive neuropsychological assessment, and measures of abnormal slow-wave activity from MEG were collected. Results demonstrated significant group differences on measures of executive functioning and processing speed. In addition, significant correlations between slow-wave activity on MEG and patterns of cognitive functioning were found in cortical areas, consistent with cognitive impairments on exams. Results provide more objective evidence that there may be subtle changes to the neurobiological integrity of the brain that can be detected by MEG. Further, these findings suggest that these abnormalities are associated with cognitive outcomes and may account, at least in part, for long-term PCS in those who have sustained an mTBI.

Keywords: executive functioning; magnetoencephalography (MEG); mild traumatic brain injury (mTBI); neuropsychological testing; postconcussive syndrome (PCS).

Figures

FIG. 1.

Images are displayed right on left, using the Harvard-Oxford Cortical Structural Atlas from FSL 4.1.3 for reference. Dark blue regions focused on in (a)–(i) demonstrate significant regions that have passed false discovery rate (FDR) correction (indicated by green arrow) associated with a negative correlation between slow-wave root mean square (RMS) amplitude and performance on Delis-Kaplan Executive Function System (D-KEFS) Color Word Interference Inhibition Scaled (i.e., poorer performance on task with higher slow-wave amplitudes). Teal regions surrounding the dark blue regions indicate where an additional cluster analysis was performed to confirm the regions that passed FDR correction. Red regions focused on in (j)–(l) demonstrate significant regions that have passed FDR correction (indicated by green arrow) associated with a positive correlation between slow-wave RMS amplitude and performance on D-KEFS Color-Word Interference Inhibition Scaled (i.e., better performance on tasks with a higher slow-wave amplitude). Yellow regions surrounding the red regions indicate where an additional cluster analysis was performed to confirm the regions that passed FDR correction. (a) Right superior/middle frontal gyrus (r=0.511). (b) Right frontal pole (r=0.462). (c) Right anterior cingulate gyrus (r=0.472). (d) Bilateral inferior parietal lobe (parietal operculum and supramarginal gyrus), left (r=0.570) and right (r=0.520). (e) Bilateral planum temporale and Heschl's gyrus, including H1 and H2, left (r=0.475) and right (r=0.567). (f) Right precuneous cortex and cingulate gyrus (r=0.547). (g) Right insular cortex (r=0.492). (h) Bilateral hippocampus and parahippocampal gyrus left (r=0.452) and right (r=0.489). (i) Left temporal fusiform/inferior temporal gyrus (r=0.507). (j) Bilateral superior parietal lobe left (r=0.452) and right (r=0.489). (k) Left frontal pole (r=0.572). (l) Left middle temporal gyrus (r=0.488). Color image is available online at www.liebertpub.com/neu

FIG. 2.

Images are displayed right on left, using the Harvard-Oxford Cortical Structural Atlas from FSL 4.1.3 for reference. (a)–(c) demonstrate significant regions (dark blue false discovery rate corrected region surrounded by additional Teal cluster analysis, indicated by green arrow) associated with a negative correlation between slow-wave root mean square amplitude and performance on Delis-Kaplan Executive Function System (D-KEFS) Trail Making Number Letter Switching Scaled (i.e., poorer performance on task with higher slow-wave amplitudes). (a) Right frontal pole (r=0.630). (b) Left frontal pole (r=0.546). (c) Right precentral gyrus (r=0.540). There were no positive correlations for this task. Color image is available online at www.liebertpub.com/neu

FIG. 3.

Images are displayed right on left, using the Harvard-Oxford Cortical Structural Atlas from FSL 4.1.3 for reference. (a) demonstrates a significant region (dark blue false discovery rate (FDR) corrected region surrounded by additional Teal cluster analysis, indicated by green arrow) associated with a negative correlation between slow-wave root mean square (RMS) amplitude and performance on Wechsler Adult Intelligence Scale (WAIS) Digit Symbol Coding Scaled (i.e., poorer performance on task with higher slow-wave amplitudes). (a) Right middle temporal gyrus/inferior temporal gyrus (r=0.568). (b)–(d) demonstrate significant regions (red FDR corrected region surrounded by additional yellow cluster analysis, indicated by green arrow) associated with a positive correlation between slow-wave RMS amplitude and performance on WAIS Digit Symbol Coding Scaled (i.e., better performance on tasks with a higher slow-wave amplitude). (b) Left superior parietal lobe/postcentral gyrus (r=0.556). (c) Right precentral gyrus (r=0.577). (d) Left frontal pole (r=0.540). Color image is available online at www.liebertpub.com/neu