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 properties 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. 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 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.