Importance of cutaneous feedback in maintaining a secure grip during manipulation of hand-held objects

Abstract

Previous research has shown that grip and load forces are modulated simultaneously during manipulation of a hand-held object. This close temporal coupling suggested that both forces are controlled by an internal model within the CNS that predicts the changes in tangential force on the fingers. The objective of the present study was to examine how the internal model would compensate for the loss of cutaneous sensation through local anesthesia of the index and thumb. Ten healthy adult subjects (5 men and 5 women aged 20-57 yr) were asked to grasp, lift, and hold stationary, a 250 g object for 20 s. Next, the subjects were asked to perform vertical oscillatory movements over a distance of 20 cm at a rate of 1.0 Hz for 30 s. Eleven trials were performed with intact sensation, and 11 trials after a local ring-block anesthesia of the index and thumb with bupivacain (5 mg/ml). During static holding, loss of cutaneous sensation produced a significant increase in the safety margin. However, the grip force declined significantly over the 20-s static hold period. During oscillatory arm movements, grip and load forces were continuously modulated together in a predictive manner as suggested by Flanagan and Wing. Again, the grip force declined over the 30-s movement, and 7/10 subjects dropped the object at least once. With intact sensation, the object was never dropped; but with the fingers anesthetized, it was dropped on 36% of the trials, and a significant slip occurred on a further 12%. The mean correlation between the grip and load forces for all subjects deteriorated from 0.71 with intact sensation to 0.48 after digital anesthesia. However, a cross-correlation calculated between the grip and load forces indicated that the phase lag was approximately zero both with and without digital anesthesia. Taken together, the data from the present study suggest that cutaneous afferents are required for setting and maintaining the background level of the grip force in addition to their phasic slip-detection function and their role in adapting the grip force/load force ratio to the friction on initial contact with an object. Finally, at a more theoretical level, they correct and maintain an internal model of the physical properties of hand-held objects.