Disturbed cortico-subcortical interactions during motor task switching in traumatic brain injury

Abstract

The ability to suppress and flexibly adapt motor behavior is a fundamental mechanism of cognitive control, which is impaired in traumatic brain injury (TBI). Here, we used a combination of functional magnetic resonance imaging and diffusion weighted imaging tractography to study changes in brain function and structure associated with motor switching performance in TBI. Twenty-three young adults with moderate-severe TBI and twenty-six healthy controls made spatially and temporally coupled bimanual circular movements. A visual cue signaled the right hand to switch or continue its circling direction. The time to initiate the switch (switch response time) was longer and more variable in the TBI group and TBI patients exhibited a higher incidence of complete contralateral (left hand) movement disruptions. Both groups activated the basal ganglia and a previously described network for task-set implementation, including the supplementary motor complex and bilateral inferior frontal cortex (IFC). Relative to controls, patients had significantly increased activation in the presupplementary motor area (preSMA) and left IFC, and showed underactivation of the subthalamic nucleus (STN) region. This altered functional engagement was related to the white matter microstructural properties of the tracts connecting preSMA, IFC, and STN. Both functional activity in preSMA, IFC, and STN, and the integrity of the connections between them were associated with behavioral performance across patients and controls. We suggest that damage to these key pathways within the motor switching network because of TBI, shifts the patients toward the lower end of the existing structure-function-behavior spectrum.

Figure 1

Task performance in the MRI scanner. (A) Subject position and custom MRI compatible joysticks are shown. Visual stimuli were projected onto a screen that occluded vision below the shoulders and were viewed via a 45° mirror. Two circles and a central fixation cross were always visible. Imperative (green arrows) and confirmation cues (white arrows) were presented for 800 ms, separated by 4 s. Switching from symmetric to asymmetric (SW»ASYMM) or from asymmetric to symmetric (SW»SYMM) movement patterns required the right hand to change circling direction: Clockwise (CW) or counter‐clockwise (CCW). (B) Representative trace from one participant performing symmetric circles followed by a switch to asymmetric circles (LH: left hand and RH: right hand). Top: Left‐ and right‐hand joystick displacement, bottom: Radial velocity plotted against time (positive radial velocity = CW circles, negative radial velocity = CCW circles). The trace segments in dark gray highlight the right‐hand switch and contralateral disruption of the left hand. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 2

Behavioral results. Top left: SwRT of the right hand. Top right: SwRT variability. Bottom left: Disruptions of contralateral (left) hand during right hand switches. Bottom right: Duration of partial contralateral disruptions. The combination of the pattern (SW»SYMM; SW»ASYMM) and switch direction (CW; CCW) determined the resulting movement pattern after the right hand switch. Results are reported as mean and 95% confidence interval of the population.

Figure 3

Event‐related analysis of Switch > Continue. Coronal sections. Yellow: Conjunction TBI ∩ Controls. Red: distinct activation in TBI. Green: distinct activation in the controls. Activations survived correction for multiple comparisons (RFX analysis, cluster level corrected at FWE P < 0.05). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 4

Statistical parametric maps showing regions with differential switch related activity between TBI patients and controls. On the left, increased activity in left IFC and preSMA in TBI, superimposed on a coronal (left) and a sagittal (middle) slice. On the right, decreased activity in STN in TBI, superimposed on a coronal slice. ROI analysis, voxel level corrected at FWE P < 0.05. (B) Pearson correlation (two‐tailed) across all participants between percent signal change (PSC) in left IFC and STN, and left preSMA and STN. (C) Pearson correlation (two‐tailed) across all participants between PSC in left preSMA and SwRT. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 5

Voxels with significantly reduced FA in the TBI group (TFCE correction) overlaid on mean FA image. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 6

(A) 3D render shows probabilistic tracts (> 95% of participants) from l‐IFC to l‐preSMA (blue), l‐IFC to l‐STN (light blue), l‐preSMA to l‐STN (green), and r‐preSMA to r‐STN (red). Coronal and sagittal sections further outline the trajectory of the individual tracts. (B) Pearson correlation (one‐tailed) across all participants between mean FA values derived from l‐IFC to l‐preSMA tract and SwRT. (C) Pearson correlation (one‐tailed) across all participants between mean FA values derived from l‐IFC to l‐preSMA tract and the percent signal change in left preSMA. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]