The Myelin Content of the Human Precentral Hand Knob Reflects Interindividual Differences in Manual Motor Control at the Physiological and Behavioral Level

Abstract

The primary motor cortex hand area (M1 _HAND) and adjacent dorsal premotor cortex (PMd) form the so-called motor hand knob in the precentral gyrus. M1 _HAND and PMd are critical for dexterous hand use and are densely interconnected via corticocortical axons, lacking a sharp demarcating border. In 24 young right-handed volunteers, we performed multimodal mapping to delineate the relationship between structure and function in the right motor hand knob. Quantitative structural magnetic resonance imaging (MRI) at 3 tesla yielded regional R1 maps as a proxy of cortical myelin content. Participants also underwent functional MRI (fMRI). We mapped task-related activation and temporal precision, while they performed a visuomotor synchronization task requiring visually cued abduction movements with the left index or little finger. We also performed sulcus-aligned transcranial magnetic stimulation of the motor hand knob to localize the optimal site (hotspot) for evoking a motor evoked potential (MEP) in two intrinsic hand muscles. Individual motor hotspot locations varied along the rostrocaudal axis. The more rostral the motor hotspot location in the precentral crown, the longer were corticomotor MEP latencies. “Hotspot rostrality” was associated with the regional myelin content in the precentral hand knob. Cortical myelin content also correlated positively with task-related activation of the precentral crown and temporal precision during the visuomotor synchronization task. Together, our results suggest a link among cortical myelination, the spatial cortical representation, and temporal precision of finger movements. We hypothesize that the myelination of cortical axons facilitates neuronal integration in PMd and M1 _HAND and, hereby, promotes the precise timing of movements.

SIGNIFICANCE STATEMENT Here we used magnetic resonance imaging and transcranial magnetic stimulation of the precentral motor hand knob to test for a link among cortical myelin content, functional corticomotor representations, and manual motor control. A higher myelin content of the precentral motor hand knob was associated with more rostral corticomotor presentations, with stronger task-related activation and a higher precision of movement timing during a visuomotor synchronization task. We propose that a high precentral myelin content enables fast and precise neuronal integration in M1 (primary motor cortex) and dorsal premotor cortex, resulting in higher temporal precision during dexterous hand use. Our results identify the degree of myelination as an important structural feature of the neocortex that is tightly linked to the function and behavior supported by the cortical area.