Direction-dependent neural control of finger dexterity in humans

Abstract

Humans, more than all other species, skillfully flex and extend their fingers to perform delicate motor tasks. This unique dexterous ability is a product of the complex anatomical properties of the human hand and the neural mechanisms that control it. Yet, the neural basis that underlies human dexterous hand movement remains unclear. Here we characterized individuation (fine control) and strength (gross control) during flexion and extension finger movements, isolated the peripheral passive mechanical coupling component from the central neuromuscular activity involved in dexterity and then applied voxel-based lesion mapping in first-event sub-acute stroke patients to investigate the causal link between the neural substrates and the behavioral aspects of finger dexterity. We found substantial differences in dexterous behavior, favoring finger flexion over extension. These differences were not caused by peripheral factors but were rather driven by central origins. Lesion-symptom mapping identified a critical brain region for finger individuation within the primary sensory-motor cortex (M1, S1), the premotor cortex (PMC), and the corticospinal (CST) fibers that descend from them. Although there was a great deal of overlap between individuated flexion and extension, we were able to identify distinct areas within this region that were associated exclusively with finger flexion. This flexion-biased differential premotor and motor cortical organization was associated with the finger individuation component, but not with finger strength. Conversely, lesion mapping revealed slight extension-biases in finger strength within descending tracts of M1. From these results we propose a model that summarizes the distinctions between individuation and strength and between finger movement in flexion and extension, revealed in human manual dexterity.