Delayed feedback during sensorimotor learning selectively disrupts adaptation but not strategy use

Abstract

Brudner SN, Kethidi N, Graeupner D, Ivry RB, Taylor JA. Delayed feedback during sensorimotor learning selectively disrupts adaptation but not strategy use. J Neurophysiol 115: 1499 -1511, 2016. First published January 20, 2016 doi:10.1152/jn.00066.2015.-In sensorimotor adaptation tasks, feedback delays can cause significant reductions in the rate of learning. This constraint is puzzling given that many skilled behaviors have inherently long delays (e.g., hitting a golf ball). One difference in these task domains is that adaptation is primarily driven by error-based feedback, whereas skilled performance may also rely to a large extent on outcome-based feedback. This difference suggests that error-and outcome-based feedback may engage different learning processes, and these processes may be associated with different temporal constraints. We tested this hypothesis in a visuomotor adaptation task. Error feedback was indicated by the terminal position of a cursor, while outcome feedback was indicated by points. In separate groups of participants, the two feedback signals were presented immediately at the end of the movement, after a delay, or with just the error feedback delayed. Participants learned to counter the rotation in a similar manner regardless of feedback delay. However, the aftereffect, an indicator of implicit motor adaptation, was attenuated with delayed error feedback, consistent with the hypothesis that a different learning process supports performance under delay. We tested this by employing a task that dissociates the contribution of explicit strategies and implicit adaptation. We find that explicit aiming strategies contribute to the majority of the learning curve, regardless of delay; however, implicit learning, measured over the course of learning and by aftereffects, was significantly attenuated with delayed error-based feedback. These experiments offer new insight into the temporal constraints associated with different motor learning processes.forward model; internal model; motor adaptation; motor learning; reinforcement learning LEARNING TO LINK ACTIONS with their respective outcomes is necessary for successfully interacting with the world. Feedback delays can present a significant problem in learning actionoutcome associations, yet such delays are ubiquitous in motor control. Feedback from proprioception and vision are inherently delayed because of neural transmission and integration time. Even if these delays are relatively short, the control system faces a significant problem due to potentially destabilizing effects arising from body and environmental dynamics.One prominent solution for handling delayed feedback in the sensorimotor learning literature centers on the idea of an adaptive forward model, a representation that allows the system to anticipate or predict the sensory consequences of an action through sensory-prediction errors (Wolpert and Miall 1996). However, various lines of evidence indicate that this solution is subject to severe temporal constraints. Modest additional delays ...

Structural Learning in a Visuomotor Adaptation Task Is Explicitly Accessible

“…Overall, our results provide further support for the general consensus that explicit re-aiming is an essential component of sensorimotor learning in a visuomotor rotation task and may be responsible for a variety of motor learning behaviors thought to be largely implicit (Heuer and Hegele, 2008; Hegele and Heuer, 2010; Taylor et al, 2014; Bond and Taylor, 2015; McDougle et al, 2015; Morehead et al, 2015; Brudner et al, 2016; Day et al, 2016; Poh et al, 2016). There are two primary implications of our results.…”

“…However, this interpretation stands in contrast to a recent series of findings demonstrating that explicitly accessible re-aiming processes constitute the majority of learning (Heuer and Hegele, 2008; Hegele and Heuer, 2010; Taylor et al, 2014; Bond and Taylor, 2015; McDougle et al, 2015; Brudner et al, 2016; Day et al, 2016; Poh et al, 2016). We previously found that explicit re-aiming composed the flexible component of performance across a range of rotation magnitudes while implicit recalibration exhibited a stereotyped response (Bond and Taylor, 2015).…”

Exposure to auditory feedback delay while speaking induces perceptual habituation but does not mitigate the disruptive effect of delay on speech auditory-motor learning

“…Consequently, task differences in the involvement of implicit vs. explicit learning mechanisms may play a role in the differential effects of sensory delays on speech and limb adaptation. This suggestion is consistent with recent work showing that, in upper limb motor learning, feedback delays negatively affect implicit learning but not explicit strategy selection (Brudner et al 2016;McDougle and Taylor 2019;Schween and Hegele 2017). It follows, then, that feedback delays may have only a relatively minor impact on visuomotor reach adaptation because it is characterized by a small implicit component and a large explicit component, at least in the case of an abruptly introduced perturbation (Anguera et al 2010;Fernandez-Ruiz et al 2011;McDougle et al 2016;Taylor et al 2014) or a gradually introduced perturbation with reward feedback (Holland et al 2018).…”

“…Indeed, several studies on speech sensorimotor learning have demonstrated that subjects are unaware that they made any changes in their speech output in the presence of the perturbation, and that there is no difference in the extent of adaptation when subjects are instructed to ignore the feedback or to avoid compensating for the perturbation (Keough et al 2013;Kim and Max 2020;Munhall et al 2003). In light of recent findings that delayed feedback may negatively affect implicit learning without much impact on explicit strategy selection (Brudner et al 2016;McDougle and Taylor 2019;Schween and Hegele 2017), speech auditory-motor learning may be resistant to the benefits of prior delay habituation due to being largely implicit in nature (Keough et al 2013;Kim and Max 2020;Munhall et al 2003). By purposefully designing new speech auditory-motor learning paradigms that depend to varying degrees on implicit vs. explicit learning, future studies might be able to directly test this hypothesis.…”

The Cerebellum: Adaptive Prediction for Movement and Cognition

“…Indeed, supervised learning is a hallmark of cerebellar function, driven by the sensory prediction error signal [42]. Notably, this signal is temporally constrained; slight delays in the delivery of an error signal markedly reduce the rate of learning [162, 163], a constraint that is much weaker in basal ganglia-dependent, reinforcement learning [164]. The exquisite temporal precision of cerebellar processing may be a key characteristic to differentiate cerebellar processing from that in the cerebral cortex [165].…”