Explicit and Implicit Contributions to Learning in a Sensorimotor Adaptation Task

Abstract

Visuomotor adaptation has been thought to be an implicit process that results when a sensory-prediction error signal is used to update a forward model. A striking feature of human competence is the ability to receive verbal instructions and employ strategies to solve tasks; such explicit processes could be used during visuomotor adaptation. Here, we used a novel task design that allowed us to obtain continuous verbal reports of aiming direction while participants learned a visuomotor rotation. We had two main hypotheses: the contribution of explicit learning would be modulated by instruction and the contribution of implicit learning would be modulated by the form of error feedback. By directly assaying aiming direction, we could identify the time course of the explicit component and, via subtraction, isolate the implicit component of learning. There were marked differences in the time courses of explicit and implicit contributions to learning. Explicit learning, driven by target error, was achieved by initially large then smaller explorations of aiming direction biased toward the correct solution. In contrast, implicit learning, driven by a sensory-prediction error, was slow and monotonic. Continuous error feedback reduced the amplitude of explicit learning and increased the contribution of implicit learning. The presence of instruction slightly increased the rate of initial learning and only had a subtle effect on implicit learning. We conclude that visuomotor adaptation, even in the absence of instruction, results from the interplay between explicit learning driven by target error and implicit learning of a forward model driven by prediction error.

Formation of a long-term memory for visuomotor adaptation following only a few trials of practice

“…How can a long-term memory for adaptation be established if not via gradual processes requiring practice at asymptote? Recent evidence showing that explicit processes contribute to initial adaptation (Taylor et al 2014;Redding and Wallace 2003;Benson et al 2011;FernandezRuiz et al 2011) may provide a possible explanation. Specifically, since an explicit aiming component is present early in adaptation (Taylor et al 2014), subjects might form a memory for this aiming strategy early during the initial exposure and recall it once they have identified that the rotation is present when tested again later.…”

“…This task is ostensibly similar to visuomotor adaptation, given that both show signs of long-term memory formation following only brief periods of initial practice (Gordon et al 1993;Flanagan and Beltzner 2000;Flanagan et al 2008). However, visuomotor adaptation is known to be subserved by both explicit and implicit processes (Mazzoni and Krakauer 2006;Taylor et al 2014), while adjustment of grip and load forces during lifting seems to be largely implicit, evidenced by the fact that the size-weight illusion persists after appropriate motor adjustments have been made (Flanagan and Beltzner 2000). These tasks also differ in their dependence on the cerebellum; patients with cerebellar degeneration are impaired in adapting to visuomotor rotations (Martin et al 1996;Maschke et al 2004;Smith and Shadmehr 2005;Chen et al 2006;Tseng et al 2007;Rabe et al 2009b) but show no apparent deficit in adjusting grip and load forces to objects of unusual densities (Rabe et al 2009a).…”

“…Alternatively, subjects may form a memory for action (Huang et al 2011;Xivry and Lefévre 2015), as opposed to a memory for an aiming direction (Taylor et al 2014), or a memory for the perturbation (Herzfeld et al 2014). We have previously suggested that this may occur through an implicit reinforcement learning mechanism that is established through experience (Huang et al 2011).…”

“…Adaptation is known to be supported by explicit processes, especially early in learning, which act in parallel with implicit, predictionerror-driven components (Redding and Wallace 2003;Mazzoni and Krakauer 2006;Keisler and Shadmehr 2010;Benson et al 2011;Taylor and Ivry 2011;Taylor et al 2014). This explicit process may involve, for instance, choosing to aim in a direction other than towards the target when adapting to a rotation (Taylor et al 2014). Thus savings may plausibly result from recall of this explicit component of prior learning, rather than modulation of the implicit one.…”

Evidence for distinct brain networks in the control of rule-based motor behavior

“…In the current study, the online correction phase of movement was less affected during the complex dual task. Because continuous visual feedback is crucial for automatic visuomotor adaptation (Hinder et al 2010;Taylor et al 2014), it is probable that the more gradual learning of the visuomotor rotation toward the diagonal targets required more online updating relative to the more discrete learning of the horizontal targets. It has been suggested that a flexible interplay between explicit, rule-based learning and implicit, adaptive learning of a forward model exists during decoupled visuomotor learning (Taylor et al 2014).…”