Multisensory components of rapid motor responses to fingertip loading

Abstract

Tactile and muscle afferents provide critical sensory information for grasp control, yet the contribution of each sensory system during online control has not been clearly identified. More precisely, it is unknown how these two sensory systems participate in online control of digit forces following perturbations to held objects. To address this issue, we investigated motor responses in the context of fingertip loading, which parallels the impact of perturbations to held objects on finger motion and fingerpad deformation, and characterized surface recordings of intrinsic (first dorsal interosseous, FDI) and extrinsic (flexor digitorum superficialis, FDS) hand muscles based on statistical modeling. We designed a series of experiments probing the effects of peripheral stimulation with or without anesthesia of the finger, and of task instructions. Loading of the fingertip generated a motor response in FDI at ~60 ms following the perturbation onset, which was only driven by muscle stretch, as the ring-block anesthesia reduced the gain of the response occurring later than 90 ms, leaving responses occurring before this time unaffected. In contrast, the motor response in FDS was independent of the lateral motion of the finger. This response started at ~90 ms on average and was immediately adjusted to task demands. Altogether these results highlight how a rapid integration of partially distinct sensorimotor circuits supports rapid motor responses to fingertip loading. NEW & NOTEWORTHY To grasp and manipulate objects, the brain uses touch signals related to skin deformation as well as sensory information about motion of the fingers encoded in muscle spindles. Here we investigated how these two sensory systems contribute to feedback responses to perturbation applied to the fingertip. We found distinct response components, suggesting that each sensory system engages separate sensorimotor circuits with distinct functions and latencies.