An FMRI study of auditory orienting and inhibition of return in pediatric mild traumatic brain injury

Abstract

Studies in adult mild traumatic brain injury (mTBI) have shown that two key measures of attention, spatial reorienting and inhibition of return (IOR), are impaired during the first few weeks of injury. However, it is currently unknown whether similar deficits exist following pediatric mTBI. The current study used functional magnetic resonance imaging (fMRI) to investigate the effects of semi-acute mTBI (<3 weeks post-injury) on auditory orienting in 14 pediatric mTBI patients (age 13.50±1.83 years; education: 6.86±1.88 years), and 14 healthy controls (age 13.29±2.09 years; education: 7.21±2.08 years), matched for age and years of education. The results indicated that patients with mTBI showed subtle (i.e., moderate effect sizes) but non-significant deficits on formal neuropsychological testing and during IOR. In contrast, functional imaging results indicated that patients with mTBI demonstrated significantly decreased activation within the bilateral posterior cingulate gyrus, thalamus, basal ganglia, midbrain nuclei, and cerebellum. The spatial topography of hypoactivation was very similar to our previous study in adults, suggesting that subcortical structures may be particularly affected by the initial biomechanical forces in mTBI. Current results also suggest that fMRI may be a more sensitive tool for identifying semi-acute effects of mTBI than the procedures currently used in clinical practice, such as neuropsychological testing and structural scans. fMRI findings could potentially serve as a biomarker for measuring the subtle injury caused by mTBI, and documenting the course of recovery.

FIG. 1.

This figure presents a diagrammatic representation of the auditory orienting task. The headphones were used to present the cue (a 2000-Hz pure tone), and the target (a 1000-Hz pure tone). The stimulus onset asynchrony (SOA) between cues and targets was 200, 400, or 700 msec. Cues correctly predicted the target location on half of the trials (50% validity ratio). Participants responded to the target location by pressing a button with their right index (left target) or middle (right target) finger.

FIG. 2.

Graphs A and B show the response time (RT) in milliseconds (msec) for patients with mild traumatic brain injury (mTBI, A), and healthy controls (HC, B). In both panels, RT for valid (solid circles) and invalid (solid triangles) trials were plotted as a function of the stimulus onset asynchronies (SOA). Graph C depicts the validity effect score (RT: invalid – valid trials) for HC (white bars) and mTBI patients (black bars) at each SOA. Error bars correspond to the standard error of the mean.

FIG. 3.

This figure presents regions showing significant group differences across all task conditions, and the percent signal change (PSC) values for mild traumatic brain injury (mTBI, red bars), and healthy controls (HC, blue bars). The magnitudes of z-scores are represented by either blue or cyan coloring. Locations of the sagittal (X) and axial (Z) slices are given according to the Talairach atlas (L, left; R, right). Decreased activation for mTBI patients compared to HC was observed within the bilateral posterior cingulate gyrus (B_PCG), the left and right thalamus and basal ganglia (THAL/BG), and bilateral cerebellum (B_CRBL). Error bars correspond to the standard error of the mean.

FIG. 4.

This figure presents the regions that exhibited a significant validity×SOA interaction when mild traumatic brain injury (mTBI) and healthy controls (HC) were collapsed. The magnitudes of z-scores are represented by either red or yellow coloring. Locations of the sagittal (X) and axial (Z) slices are given according to the Talairach atlas (L, left; R, right). Percent signal change (PSC) values for the regions implicated in the interaction are presented for valid (red bars) and invalid (blue bars) trials at 200, 400, and 700 msec SOA. The areas included the bilateral pre-supplementary/supplementary motor area (B_P-SMA/SMA), the near left frontal eye fields (L_FEF), and the left inferior parietal lobe (L_IPL). Error bars correspond to the standard error of the mean (SOA, stimulus onset asynchrony).