Mild Traumatic Brain Injury Affects Cognitive Processing and Modifies Oscillatory Brain Activity during Attentional Tasks

Abstract

Despite the high prevalence of mild traumatic brain injury (mTBI), current diagnostic tools to objectively assess cognitive complaints after mTBI continue to be inadequate. Our aim was to identify neuronal correlates for cognitive difficulties in mTBI patients by evaluating the possible alterations in oscillatory brain activity during a behavioral task known to be sensitive to cognitive impairment after mTBI. We compared oscillatory brain activity during rest and cognitive tasks (Paced Auditory Serial Addition Test [PASAT] and a vigilance test [VT]) with magnetoencephalography between 25 mTBI patients and 20 healthy controls. Whereas VT induced no significant differences compared with resting state in either group, patients exhibited stronger attenuation of 8- to 14-Hz oscillatory activity during PASAT than healthy controls in the left parietotemporal cortex (p ≤ 0.05). Further, significant task-related modulation in the left superior frontal gyrus and right prefrontal cortex was detected only in patients. The ∼10-Hz (alpha) peak frequency declined in frontal, temporal, and parietal regions during PASAT compared with rest (p < 0.016) in patients, whereas in controls it remained the same or showed a tendency to increase. In patients, the ∼10-Hz peak amplitude was negatively correlated with behavioral performance in the Trail Making Test. The observed alterations in the cortical oscillatory activity during cognitive load may provide measurable neurophysiological correlates of cognitive difficulties in mTBI patients, even at the individual level.

Keywords: alpha frequency modulation; cognitive task; magnetoencephalography; mild traumatic brain injury.

FIG. 1.

Overview of the data. Sensor-level areal mean spectra for (A) control subjects and (B) patients. Inserts (right, A and B) show enlarged the mean spectra over the right parietal and occipital areas, demonstrating the activity during the tasks (VT, PASAT) compared with rest (EO). The vertical lines in the inserts mark the 8- to 14-Hz band used for source-level power mapping. EO, eyes open; VT, vigilance test; PASAT, Paced Auditory Serial Addition Test; L, left; R, right.

FIG. 2.

Alpha peak frequency modulation during the cognitive tasks (PASAT, VT) compared with rest (EO) in parietal and occipital areas, both hemispheres unified. Asterisks denote statistically significant difference: in controls between parietal and occipital areas during PASAT, and in patients between EO and PASAT tasks in parietal areas. EO, eyes open; PASAT, Paced Auditory Serial Addition Test; VT, vigilance test; SE, standard error.

FIG. 3.

Activation patterns during the PASAT. (A) Controls exhibit 8- to 14-Hz attenuation (p < 0.05, corrected) in the bilateral fronto-parieto-temporal areas during the PASAT compared with EO, whereas (B) patients show statically significant attenuation (p < 0.05, corrected) also in the dorsolateral and -medial pre-frontal cortices. (C) Between-group comparison during PASAT depicts stronger attenuation of 8- to 14-Hz power (p < 0.05, corrected) in patients than controls in the left supramarginal and angular gyri, left DLPFC, right DMPFC, bilateral precentral, and left paracentral areas. PASAT, Paced Auditory Serial Addition Test; VT, vigilance test; EO, eyes open; DLPFC, dorsolateral pre-frontal cortex; DMPFC, dorsomedial pre-frontal cortex.