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Abstract Until recently, neural assessments of gross motor coordination could not reliably handle active tasks, particularly in realistic environments, and offered a narrow understanding of motor-cognition. By applying a comprehensive neuroergonomic approach using optical mobile neuroimaging, we probed the neural correlates of motor functioning in young people with Developmental Coordination Disorder (DCD), a motor-learning deficit affecting 5–6% of children with lifelong complications. Neural recordings using fNIRS were collected during active ambulatory behavioral task execution from 37 Typically Developed and 48 DCD Children who performed cognitive and physical tasks in both single and dual conditions. This is the first of its kind study targeting regions of prefrontal cortical dysfunction for identification of neuropathophysiology for DCD during realistic motor tasks and is one of the largest neuroimaging study (across all modalities) involving DCD. We demonstrated that DCD is a motor-cognitive disability, as gross motor /complex tasks revealed neuro-hemodynamic deficits and dysfunction within the right middle and superior frontal gyri of the prefrontal cortex through functional near infrared spectroscopy. Furthermore, by incorporating behavioral performance, decreased neural efficiency in these regions were revealed in children with DCD, specifically during motor tasks. Lastly, we provide a framework, evaluating disorder impact in ecologically valid contexts to identify when and for whom interventional approaches are most needed and open the door for precision therapies.

Developmental coordination disorder (DCD) is characterized by motor learning deficits that are poorly understood within whole-body activities context. Here we present results of one of the largest non-randomized interventional trials combining brain imaging and motion capture techniques to examine motor skill acquisition and its underpinning mechanisms in adolescents with and without DCD. A total of 86 adolescents with low fitness levels (including 48 with DCD) were trained on a novel stepping task for a duration of 7 weeks. Motor performance during the stepping task was assessed under single and dual-task conditions. Concurrent cortical activation in the prefrontal cortex (PFC) was measured using functional near-infrared spectroscopy (fNIRS). Additionally, structural and functional magnetic resonance imaging (MRI) was conducted during a similar stepping task at the beginning of the trial. The results indicate that adolescents with DCD performed similarly to their peers with lower levels of fitness in the novel stepping task and demonstrated the ability to learn and improve motor performance. Both groups showed significant improvements in both tasks and under single- and dual-task conditions at post-intervention and follow-up compared to baseline. While both groups initially made more errors in the Stroop task under dual-task conditions, at follow-up, a significant difference between single- and dual-task conditions was observed only in the DCD group. Notably, differences in prefrontal activation patterns between the groups emerged at different time points and task conditions. Adolescents with DCD exhibited distinct prefrontal activation responses during the learning and performance of a motor task, particularly when complexity was increased by concurrent cognitive tasks. Furthermore, a relationship was observed between MRI brain structure and function measures and initial performance in the novel stepping task. Overall, these findings suggest that strategies that address task and environmental complexities, while simultaneously enhancing brain activity through a range of tasks, offer opportunities to increase the participation of adolescents with low fitness in physical activity and sports.