Neural correlates of fine motor grasping skills: Longitudinal insights into motor cortex activation using fNIRS

Abstract

Background: Motor learning is essential for performing specific tasks and progresses through distinct stages, including the rapid learning phase (initial skill acquisition), the consolidation phase (skill refinement), and the stable performance phase (skill mastery and maintenance). Understanding the cortical activation dynamics during these stages can guide targeted rehabilitation interventions.

Methods: In this longitudinal randomized controlled trial, functional near-infrared spectroscopy was used to explore the temporal dynamics of cortical activation in hand-related motor learning. Thirty-one healthy right-handed individuals were randomly assigned to perform either easy or intricate motor tasks with their non-dominant hand over 10 days. We conducted 10 monitoring sessions to track cortical activation in the right hemisphere (according to lateralization principles, the primary hemisphere for motor control) and evaluated motor proficiency concurrently.

Results: The study delineated three stages of nondominant hand motor learning: rapid learning (days 1 and 2), consolidation (days 3-7), and stable performance (days 8-10). There was a power-law enhancement of motor skills correlated with learning progression. Sustained activation was observed in the supplementary motor area (SMA) and parietal lobe (PL), whereas activation in the right primary motor cortex (M1R) and dorsolateral prefrontal cortex (PFCR) decreased. These cortical activation patterns exhibited a high correlation with the augmentation of motor proficiency.

Conclusions: The findings suggest that early rehabilitation interventions, such as transcranial magnetic stimulation and transcranial direct current stimulation (tDCS), could be optimally directed at M1 and PFC in the initial stages. In contrast, SMA and PL can be targeted throughout the motor learning process. This research illuminates the path for developing tailored motor rehabilitation interventions based on specific stages of motor learning.

New and noteworthy: In an innovative approach, our study uniquely combines a longitudinal design with the robustness of generalized estimating equations (GEEs). With the synergy of functional near-infrared spectroscopy (fNIRS) and the Minnesota Manual Dexterity Test (MMDT) paradigm, we precisely trace the evolution of neural resources during complex, real-world fine-motor task learning. Centering on right-handed participants using their nondominant hand magnifies the intricacies of right hemisphere spatial motor processing. We unravel the brain's dynamic response throughout motor learning stages and its potent link to motor skill enhancement. Significantly, our data point toward the early-phase rehabilitation potential of TMS and transcranial direct current stimulation on the M1 and PFC regions. Concurrently, SMA and PL appear poised to benefit from ongoing interventions during the entire learning curve. Our findings carve a path for refined motor rehabilitation strategies, underscoring the importance of timely noninvasive brain stimulation treatments.

Keywords: cortical activation; functional near-infrared spectroscopy (fNIRS); longitudinal study; motor learning; motor rehabilitation.

FIGURE 1

Minnesota manual dexterity test tasks design diagram: (a) photographic documentation from the field, (b) schematic representation of the task procedure left: one hand displacing task (D); right: one hand displacing and turning task (DaT).

FIGURE 2

Head model placement and cortical subdivisions: from left to right: horizontal channel layout, sagittal channel layout; real‐life participant wearing the device.

FIGURE 3

E‐prime program flowchart: The direction of the arrow denotes the progression of time throughout the task.

FIGURE 4

Trend of task completion time in MMDT DaT: one hand displacing and turning task group illustrated with blue solid lines; D: one hand displacing task group represented with red solid lines. Vertical axis: mean value of MMDT completion time; horizontal axis: motor learning assessment time points.

FIGURE 5

Activation trends in right hemisphere cortical areas during motor learning DaT: one hand displacing and turning task group illustrated with blue solid lines; D: one hand displacing task group represented with red solid lines. Vertical axis: The activation of the cerebral cortex was expressed as the change in blood oxygen (ΔHBO, μmol/L); horizontal axis: motor learning assessment time points; M1R, right primary motor cortex; PLR: right parietal cortex; PFCR: right dorsolateral prefrontal cortex; SMAR, right supplementary motor area;. “*” indicates p < .05, “**” indicates p < .01, “***” indicates p < .001.

FIGURE 6

Temporal fluctuations in blood oxygenation levels during cortical activation and their association with motor performance. The x‐axis represents the completion time (s) of the MMDT task for the left upper limb (learning side), and the y‐axis indicates the activation (μmol/L) of the right cortical areas during the motor learning assessment of the learning side (left upper limb). M1R, right primary motor cortex; PFCR, right dorsolateral prefrontal cortex; PLR, right parietal cortex; SMAR, right supplementary motor area.