Kinematics and end-point control of arm movements are modified by unexpected changes in viscous loading

Abstract

These experiments were undertaken to evaluate whether the kinematics and end-point control of learned movements were affected by changes in dynamic loads or were determined largely by centrally specified motor programs. Human subjects performed flexion movements about the wrist in a discrete visual tracking task for a range of movement sizes. For some movements, viscosity was increased at movement onset. When the viscous load opposed movement unexpectedly, subjects initially overshot the intended target for all movement sizes, but only for the smaller movements did the overshoot persist. Unexpected introduction of heavier loads was more effective in inducing these behavioral changes; the lightest loads did not alter end-point positioning. When subjects had visual guidance about performance when load changes occurred, the effect of the unexpected occurrences of viscous loads was diminished, suggesting that subjects rapidly adjusted their movement strategy, depending on task demands and performance. The movement responses were mediated by short-latency and long-duration muscle responses triggered by the change in viscous loading. Although the triggered muscle responses were larger when the loads were encountered during performance of large, in comparison to small, movements, smaller muscle responses affected small movements more than large triggered responses did large movements. This suggests that triggered muscle responses are compensatory in certain movement situations but disruptive in others. In addition, these findings demonstrated that dynamic loads especially affect the kinematics and end-point control of smaller movements, suggesting that kinesthetic inputs and central motor commands interact so subjects may achieve accurate positioning for certain classes of movements.Several recent studies of motor control in patients with sensory loss have described impairments of movement accuracy as a result of viscous-load changes occurring during movement (Day and Marsden, 1982;Nam et al., 1984;Rothwell et al., 1982a;Sanes et al., 1985). The reason for the use of viscous loads (as compared to springs or weights) in these studies was that viscous loads acted during displacement but not during absence of movement. Thus, if a subject is to displace the wrist from one angle to another at a fixed angular velocity, an unexpected change of viscosity will require changed muscular output during the displacement between the starting position and the terminal

Afferent Input, Efference Copy, Signal Noise, and Biases in Perception of Joint Angle During Active Versus Passive Elbow Movements

“…Transient overestimation of hand position or joint angle before and during the early part of active arm movements has been interpreted as evidence of an efference copy-based forward prediction of limb state (Ariff et al 2002;Dassonville 1995;Lonn et al 2000;Sanes 1986;Wolpert et al 1995). We also found that subjects overestimated their elbow angle early in active test movements and that they underestimated it later in the movements.…”

“…A role for efference copy in state estimation is well established in control theory and in motor control studies (Bhushan and Shadmehr 1999;Miall et al 1993;Sabes 2000;Wolpert and Kawato 1998). Evidence for a role for efference copy in kinesthetic sensation has been provided by overestimates of hand position or joint angle before and during active movements (Ariff et al 2002;Dassonville 1995;Lonn et al 2000;Sanes 1986;Wolpert et al 1995), by more accurate estimates of static position after active movements than passive movements (Adamovich et al 1998;Craske and Crawshaw 1975;Laufer et al 2001;Lonn et al 2000;Brouchon 1968, 1974;Winter et al 2005), and by perceptual deficits after cortical lesions ). The reduction of position estimation errors during active compared with passive movements in this study indicates that an efference copy improves arm state estimation during active movement.…”

“…However, state estimation based solely on afferent input during movement is problematic because of the conduction delays, which can lead to dynamic instability in the feedback control circuit. Theoretical studies propose that an "internal forward model" could reduce the instability problem by using both an efference copy of the outgoing motor command and afferent sensory signals to estimate the current or immediate future state of the limb (Bhushan and Shadmehr 1999;Miall et al 1993;Scarchilli et al 1999;Wolpert et al 1995). According to the theory, as the movement unfolds, efference copy-based predictions about future states of the limb would combine with delayed sensory feedback signals about the most recently sensed actual state of the limb to continuously update the limb state estimate.…”

“…Although originally thought to be caused by weaker proprioceptive signals generated during passive movements (Jeannerod 1988), more recent evidence suggests that this may instead result from a lack of an efference copy (Ansems et al 2006;Blakemore et al 1998;Christensen et al 2007;Jones et al 2001a). Other studies found that hand position is systematically overestimated in the direction of movement during the early part of unseen active arm movements (Ariff et al 2002;Dassonville 1995;Lonn et al 2000;Sanes 1986;Wolpert et al 1995). These error biases are consistent with the hypothesis that an efference copy of the outgoing motor command created a transient forward projection of the limb state estimate along the intended movement path before the onset of movement.…”

End Points of Planar Reaching Movements Are Disrupted by Small Force Pulses: An Evaluation of the Hypothesis of Equifinality

“…There have been several pertinent studies indicating that muscle behavior may not be simply spring-like even under full reflexive control. There is evidence that active areflexive muscle is itself not spring-like because a viscous load imposed on muscle in this condition yields a large undershoot in the final position (Lin and Rymer 1998;Rothwell et al 1982a;Sanes 1986), a finding that contradicts common beliefs about muscle spring-like properties. Furthermore muscle yield (Joyce et al 1969), which is an abrupt change in stiffness recorded once active muscle is stretched more than a fraction of a millimeter, may provide a mechanism by which even small transient loads can change muscle state, inducing further deviations from spring-like behavior.…”