Primitives for Motor Adaptation Reflect Correlated Neural Tuning to Position and Velocity

Abstract

The motor commands required to control voluntary movements under various environmental conditions may be formed by adaptively combining a fixed set of motor primitives. Since this motor output must contend with state-dependent physical dynamics during movement, these primitives are thought to depend on the position and velocity of motion. Using a recently developed "error-clamp" technique, we measured the fine temporal structure of changes in motor output during adaptation. Interestingly, these measurements reveal that motor primitives echo a key feature of the neural coding of limb motion-correlated tuning to position and velocity. We show that this correlated tuning explains why initial stages of motor learning are often rapid and stereotyped, whereas later stages are slower and stimulus specific. With our new understanding of these primitives, we design dynamic environments that are intrinsically the easiest or most difficult to learn, suggesting a theoretical basis for the rational design of improved procedures for motor training and rehabilitation.

Gain Field Encoding of the Kinematics of Both Arms in the Internal Model Enables Flexible Bimanual Action

“…To quantify the degree of motor adaptation when changing movement directions of both arms (see Fig. 1B for the definition of "movement direction"), we used the "error-clamp" method (Scheidt et al, 2000;Smith et al, 2006;Sing et al, 2009). During error-clamped trials, the trajectory of the handle was constrained to a straight line toward the target by a virtual "channel" (see Fig.…”

“…Previous studies of unimanual reaching movement have suggested that the brain accomplishes flexible movements by constructing an "internal model" of the dynamic properties of the body and the environment (Kawato, 1989;Bhushan and Shadmehr, 1999). It was also suggested that humans build these internal models through a flexible combination of motor primitives encoding the kinematics of the desired arm (Thoroughman and Shadmehr, 2000;Donchin et al, 2003;Sing et al, 2009). However, this powerful scheme is not directly compatible with control of bimanual movement.…”

“…This close similarity to the current problem led us to further hypothesize that multiplicative encoding of the kinematics of both arms in the primitives enables the brain to create an arbitrary force output. We tested this hypothesis by examining the generalization pattern of motor learning (Shadmehr and Mussa-Ivaldi, 1994; Thorough-man and Shadmehr, 2000;Donchin et al, 2003;Hwang et al, 2003;Sing et al, 2009), which should reflect the encoding structure in the primitives (Hwang et al, 2003;Wainscott et al, 2005).…”

Adaptation Paths to Novel Motor Tasks Are Shaped by Prior Structure Learning

“…The session on the last day consisted of continuing exposure to the horizontal/vertical force fields, interspersed with four probing batches. Each probing batch (always preceded by a 10 trial washout) consisted of 20 probing "triplets" (Sing et al, 2009) with three to five washout trials in between. Each triplet consisted of an error-clamp trial without any additional force field, followed by a velocity-dependent force field trial with a force in one of the four diagonal direction and a gain of 5 N ⅐ s/m, and another errorclamp trial without additional force field.…”

“…On the third day, we tested how subjects adapted to diagonal force fields by using triplets of trials, consisting of a diagonal force field trial with the gain of 5 N ⅐ s/m, sandwiched between two error-clamp trials (Sing et al, 2009). These triplets were separated by three to five washout trials (no force, no error clamp), and every subject experienced 80 triplets in total, with 20 triplets using forces in each diagonal direction.…”