Preparing to Reach: Selecting an Adaptive Long-Latency Feedback Controller

Abstract

In a voluntary movement, the nervous system specifies not only the motor commands, but also the gains associated with reaction to sensory feedback. For example, suppose that during reaching a perturbation tends to push the hand to the left. With practice, the brain not only learns to produce commands that predictively compensate for the perturbation, but also increases the long-latency reflex gain associated with leftward displacements of the arm. That is, the brain learns a feedback controller. Here, we wondered whether during the preparatory period before the reach the brain engaged this feedback controller in anticipation of the upcoming movement. If so, its signature might be present in how the motor system responds to perturbations in the preparatory period. Humans trained on a reach task in which they adapted to a force field. During the preparatory period before the reach we measured how the arm responded to a pulse to the hand that was either in the direction of the upcoming field, or in the opposite direction. Reach adaptation produced an increase in the long-latency (45–100ms delay) feedback gains with respect to baseline, but only for perturbations that were in the same direction as the force field that subjects expected to encounter during the reach. Therefore, as the brain prepares for a reach, it loads a feedback controller specific to the upcoming reach. With adaptation, this feedback controller undergoes a change, increasing the gains for the expected sensory feedback.

Contributions of the cerebellum and the motor cortex to acquisition and retention of motor memories

“…While there are many factors that can affect kinematic performance in field trials, including changes in muscle co-contraction (Thoroughman and Shadmehr, 1999), and changes in the gain of the long-latency sensory feedback pathways (Kimura et al, 2006; Kimura and Gomi, 2009; Ahmadi-Pajouh et al, 2012), in error-clamp trials these factors are eliminated. Forces that participants produce in error-clamp trials are a proxy for a model that the brain constructs, associating state of the limb to expected perturbation forces (Hwang and Shadmehr, 2005; Sing et al, 2009).…”

Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration

“…This may be critically important, since movement trajectory is affected both by the ability of the nervous system to learn from errors that were observed in the previous trials, termed trial-to-trial learning, and respond to errors that are sensed in the current trial, termed within-trial response to error (Ahmadi-Pajouh et al 2012;Franklin et al 2007;Kimura et al 2006;Kimura and Gomi 2009;Wong et al 2009). Some studies suggest that the human motor cortex may play an important role in learning to modulate the within-trial response to error (Kimura et al 2006), although disruption of the human cerebellum also reduces the gain of this feedback pathway (Herzfeld et al 2014a).…”

Rapid Feedback Responses Correlate with Reach Adaptation and Properties of Novel Upper Limb Loads

“…Our results compliment previous work highlighting feedback corrections that are altered by training with novel hand forces (Wagner and Smith, 2008;Kimura and Gomi, 2009;Yousif and Diedrichsen, 2012). Adaptive stretch responses have even been found during the preparatory period before reach onset (Ahmadi-Pajouh et al, 2012), suggesting that reach adaptation may have the capability to alter corrective responses engaged for postural control. This transfer of learning may reflect the partial overlap in neural control across reaching and posture tasks (Kurtzer et al, 2005).…”

“…This "automatic gain-scaling" effect has made it difficult to isolate adapted stretch responses from automatic spinal processes engaged during the ongoing movement. As a result, changes in feedback responses during adaptation have only indirectly been measured in postural control before movement onset (Ahmadi-Pajouh et al, 2012) or by perturbing visual feedback . A key challenge for exploring how motor adaptation influences feedback responses will be to develop techniques where the level of muscle activity is unaltered by the adaptation process.…”