Lukos JR, Choi JY, Santello M. Grasping uncertainty: effects of sensorimotor memories on high-level planning of dexterous manipulation. J Neurophysiol 109: 2937-2946, 2013. First published April 3, 2013 doi:10.1152/jn.00060.2013.-For successful object manipulation, the central nervous system must appropriately coordinate digit placement and force distribution. It is known that digit force planning is significantly influenced by previous manipulations even when object properties cannot be predicted on a trial-to-trial basis. We sought to determine whether this effect extends beyond force control to the coordination of digit placement and force. Subjects grasped and lifted an object whose center of mass (CM) was changed unpredictably across trials. Grasp planning was quantified by measuring the torque generated on the object at lift onset. We found that both digit placement and force were systematically affected by the CM experienced on the previous trial. Additionally, the negative covariation between digit forces and positions typically found for predictable CM presentations was also found for unpredictable CM trials. A follow-up experiment revealed that these effects were not dependent on visual feedback of object roll during object lift on the previous trial. We conclude that somatosensory feedback from previous grasp experience alone can affect high-level grasp planning by constraining the relation between digit force and position even when the task behavioral consequences cannot be reliably predicted. As learning of manipulations often involves interactions with objects in novel environments, the present findings are an important step to understanding the control strategies associated with the integration of sensorimotor memories and motor planning.

Recent studies about sensorimotor control of the human hand have focused on how dexterous manipulation is learned and generalized. Here we address this question by testing the extent to which learned manipulation can be transferred when the contralateral hand is used and/or object orientation is reversed. We asked subjects to use a precision grip to lift a grip device with an asymmetrical mass distribution while minimizing object roll during lifting by generating a compensatory torque. Subjects were allowed to grasp anywhere on the object’s vertical surfaces, and were therefore able to modulate both digit positions and forces. After every block of eight trials performed in one manipulation context (i.e., using the right hand and at a given object orientation), subjects had to lift the same object in the second context for one trial (transfer trial). Context changes were made by asking subjects to switch the hand used to lift the object and/or rotate the object 180° about a vertical axis. Therefore, three transfer conditions, hand switch (HS), object rotation (OR), and both hand switch and object rotation (HS+OR), were tested and compared with hand matched control groups who did not experience context changes. We found that subjects in all transfer conditions adapted digit positions across multiple transfer trials similar to the learning of control groups, regardless of different changes of contexts. Moreover, subjects in both HS and HS+OR group also adapted digit forces similar to the control group, suggesting independent learning of the left hand. In contrast, the OR group showed significant negative transfer of the compensatory torque due to an inability to adapt digit forces. Our results indicate that internal representations of dexterous manipulation tasks may be primarily built through the hand used for learning and cannot be transferred across hands.

Dexterous manipulation relies on modulation of digit forces as a function of digit placement. However, little is known about the sense of position of the vertical distance between finger pads relative to each other. We quantified subjects' ability to match perceived vertical distance between the thumb and index finger pads (dy) of the right hand (“reference” hand) using the same or opposite hand (“test” hand) after a 10-second delay without vision of the hands. The reference hand digits were passively placed non-collinearly so that the thumb was higher or lower than the index finger (dy = 30 or –30 mm, respectively) or collinearly (dy = 0 mm). Subjects reproduced reference hand dy by using a congruent or inverse test hand posture while exerting negligible digit forces onto a handle. We hypothesized that matching error (reference hand dy minus test hand dy) would be greater (a) for collinear than non-collinear dys, (b) when reference and test hand postures were not congruent, and (c) when subjects reproduced dy using the opposite hand. Our results confirmed our hypotheses. Under-estimation errors were produced when the postures of reference and test hand were not congruent, and when test hand was the opposite hand. These findings indicate that perceived finger pad distance is reproduced less accurately (1) with the opposite than the same hand and (2) when higher-level processing of the somatosensory feedback is required for non-congruent hand postures. We propose that erroneous sensing of finger pad distance, if not compensated for during contact and onset of manipulation, might lead to manipulation performance errors as digit forces have to be modulated to perceived digit placement.