Neuroplasticity of cognitive control networks following cognitive training for chronic traumatic brain injury

Abstract

Cognitive control is the ability to coordinate thoughts and actions to achieve goals. Cognitive control impairments are one of the most persistent and devastating sequalae of traumatic brain injuries (TBI). There have been efforts to improve cognitive control in individuals with post-acute TBI. Several studies have reported changes in neuropsychological measures suggesting the efficacy of cognitive training in improving cognitive control. Yet, the neural substrates of improved cognitive control after training remains poorly understood. In the current study, we identified neural plasticity induced by cognitive control training for TBI using resting-state functional connectivity (rsFC). Fifty-six individuals with chronic mild TBI (9 years post-injury on average) were randomized into either a strategy-based cognitive training group (N = 26) or a knowledge-based training group (active control condition; N = 30) for 8 weeks. We acquired a total of 109 resting-state functional magnetic resonance imaging from 45 individuals before training, immediately post-training, and 3 months post-training. Relative to the controls, the strategy-based cognitive training group showed monotonic increases in connectivity in two cognitive control networks (i.e., cingulo-opercular and fronto-parietal networks) across time points in multiple brain regions (p_voxel < 0.001, p_cluster < 0.05). Analyses of brain-behavior relationships revealed that fronto-parietal network connectivity over three time points within the strategy-based cognitive training group was positively associated with the trail making scores (p_voxel < 0.001, p_cluster < 0.05). These findings suggest that training-induced neuroplasticity continues through chronic phases of TBI and that rsFC can serve as a neuroimaging biomarker of evaluating the efficacy of cognitive training for TBI.

Keywords: Cognitive control; Cognitive function; Neuroplasticity; Rehabilitation; Resting-state functional connectivity; Traumatic brain injury.

Fig. 1

Seed locations. Black and yellow circles represent seeds for the cingulo-opercular network and fronto-parietal network, respectively. aI/fO, anterior insula/frontal operculum; aPFC, anterior prefrontal cortex; dACC, dorsal anterior cingulate cortex; dFC, dorsal frontal cortex; dlPFC, dorsolateral prefrontal cortex; IPS; intraparietal sulcus; mCC, middle cingulate cortex; PCUN, precuneus; L, left; R, right.

Fig. 2

Neuropsychological assessment results. TP₁, Prior to training; TP₂, After training; TP₃, 3 months later; SMART, Strategic Memory Advanced Reasoning Training; BHW, Brain Health Workshop.

Fig. 3

Between-group contrast maps for changes in connectivity over time. See Fig. 1, Fig. 2 for abbreviations.

Fig. 4

Within-group contrast maps for changes in connectivity over time.

Fig. 5

Colormaps for between-group contrast for temporal changes in connectivity according to the patterns of within-group changes.

Fig. 6

Colormaps for temporal changes in connectivity relative to baseline connectivity.

Fig. 7

Composite maps across seeds. A: Foci maps. B: Connectivity overlap across seeds, C: Colormaps for temporal changes in connectivity according to the cognitive control networks. D: The Yeo atlas of large-scale resting-state networks (Yeo et al., 2011). E: The counts of voxels with statistically significant changes in connectivity according to the resting-state networks. SCG, subcentral gyrus; vlPFC, ventrolateral prefrontal cortex; STG, superior temporal gyurs; MT+, middle temporal complex; VN, visual network; SMN, somatomotor network; DAN, dorsal attention network; CON, cingulo-opercular network; LN, limbic network; FPN, fronto-parietal network; DMN, default mode network. See Fig. 1 for the other abbreviations.

Fig. 8

Associations between the average L dlPFC connectivity and average scores of the trail making test over time. Top row: Colormaps for statistically significant associations between the two measures. Other rows: Average L dlFPC connectivity versus average trail making scores within each of the clusters in the top row. Each colored triangle (circle) represents average L dlPFC and trail making score of each individual from the SMART (BHW) group, and black symbol represents group-averaged trajectory in the regions. dPFC, dorsal prefrontal cortex; AG, angular gyrus; PCC, posterior cingulate cortex. See Fig. 1, Fig. 2 for the other abbreviations.

Fig. 9

Associations between temporal changes in the trail making scores and changes in connectivity with L dFC. Top row: Colormaps for statistically significant associations between the two measures. Bottom row: Trajectories of each individuals (colored line) and group average (black line). See Fig. 1, Fig. 2, Fig. 8 for the other abbreviations.