Evolution of object identity information in sensorimotor cortex throughout grasp

ABSTRACT The transition from hand opening to grasping a coffee cup happens smoothly, yet the neural systems underlying this behavior undergo a significant state change at the onset of grasp. At this moment, the motor system begins to control contact forces and the somatosensory system receives a barrage of cutaneous signals that convey information about contact forces and the object’s local features (e.g., edges, texture, and curvature). These cutaneous signals supplement the ongoing flow of proprioceptive input that encodes hand posture as well as muscle forces. How object identity is represented in sensorimotor cortex across this transition remains unknown. In the present study, we sought to quantify the object-specific neural signals in individual neurons of the primary motor cortex (M1) and Brodmann areas 3a, 3b/1, and 2 of the somatosensory cortex in macaque monkeys. Before contact, object-specific information was carried mainly by M1 and proprioceptive area 3a, but this information did not generalize between the periods before and after contact. This observation is consistent with the abruptly changing force signals at contact affecting the assumed postural representation of the object, rather than each modality maintaining an invariant identity. After contact, despite a general decrease in firing rates, information about object identity increased and was encoded with high efficiency across sensorimotor cortex. Cutaneous areas 3b and 1, largely uninformative before contact, became highly informative once objects were grasped. Area 2, which receives both cutaneous and musculotendinous inputs, conveyed little object-specific information before contact, when it too became strongly informative, consistent with its integrative role. Thus, M1 and 3a serve as the main carriers of object information before contact, while cutaneous and integrative somatosensory circuits dominate after contact. This shift highlights the profound change in the coding of object identify in the sensorimotor cortex during contact.