Neural Representations of Sensorimotor Memory- and Digit Position-Based Load Force Adjustments Before the Onset of Dexterous Object Manipulation.

Abstract

Anticipatory load forces for dexterous object manipulation in humans are modulated based on visual object property cues, sensorimotor memories of previous experiences with the object, and, when digit positioning varies from trial to trial, the integrating of this sensed variability with force modulation. Studies of the neural representations encoding these anticipatory mechanisms have not considered these mechanisms separately from each other or from feedback mechanisms emerging after lift onset. Here, representational similarity analyses of fMRI data were used to identify neural representations of sensorimotor memories and the sensing and integration of digit position. Cortical activity and movement kinematics were measured as 20 human subjects (11 women) minimized tilt of a symmetrically shaped object with a concealed asymmetric center of mass (CoM, left and right sided). This task required generating compensatory torques in opposite directions, which, without helpful visual CoM cues, relied primarily on sensorimotor memories of the same object and CoM. Digit position was constrained or unconstrained, the latter of which required modulating forces beyond what can be recalled from sensorimotor memories to compensate for digit position variability. Ventral premotor (PMv), somatosensory, and cerebellar lobule regions (CrusII, VIIIa) were sensitive to anticipatory behaviors that reflect sensorimotor memory content, as shown by larger voxel pattern differences for unmatched than matched CoM conditions. Cerebellar lobule I-IV, Broca area 44, and PMv showed greater voxel pattern differences for unconstrained than constrained grasping, which suggests their sensitivity to monitor the online coincidence of planned and actual digit positions and correct for a mismatch by force modulation.SIGNIFICANCE STATEMENT To pick up a water glass without slipping, tipping, or spilling requires anticipatory planning of fingertip load forces before the lift commences. This anticipation relies on object visual properties (e.g., mass/mass distribution), sensorimotor memories built from previous experiences (especially when object properties cannot be inferred visually), and online sensing of where the digits are positioned. There is limited understanding of how the brain represents each of these anticipatory mechanisms. We used fMRI measures of regional brain patterns and digit position kinematics before lift onset of an object with nonsalient visual cues specifically to isolate sensorimotor memories and integration of sensed digit position with force modulation. In doing so, we localized neural representations encoding these anticipatory mechanisms for dexterous object manipulation.