Reexposure to a sensorimotor perturbation produces opposite effects on explicit and implicit learning processes

Abstract

The motor system demonstrates an exquisite ability to adapt to changes in the environment and to quickly reset when these changes prove transient. If similar environmental changes are encountered in the future, learning may be faster, a phenomenon known as savings. In studies of sensorimotor learning, a central component of savings is attributed to the explicit recall of the task structure and appropriate compensatory strategies. Whether implicit adaptation also contributes to savings remains subject to debate. We tackled this question by measuring, in parallel, explicit and implicit adaptive responses in a visuomotor rotation task, employing a protocol that typically elicits savings. While the initial rate of learning was faster in the second exposure to the perturbation, an analysis decomposing the 2 processes showed the benefit to be solely associated with explicit re-aiming. Surprisingly, we found a significant decrease after relearning in aftereffect magnitudes during no-feedback trials, a direct measure of implicit adaptation. In a second experiment, we isolated implicit adaptation using clamped visual feedback, a method known to eliminate the contribution of explicit learning processes. Consistent with the results of the first experiment, participants exhibited a marked reduction in the adaptation function, as well as an attenuated aftereffect when relearning from the clamped feedback. Motivated by these results, we reanalyzed data from prior studies and observed a consistent, yet unappreciated pattern of attenuation of implicit adaptation during relearning. These results indicate that explicit and implicit sensorimotor processes exhibit opposite effects upon relearning: Explicit learning shows savings, while implicit adaptation becomes attenuated

Non-invasive stimulation of the motor cerebellum has potential cognitive confounds

“…through modifying explicit mechanisms such as the use of strategies [16]), or an interplay between both circuits (see also [17]). This could potentially explain the difficulties seen in studies attempting to separately modulate the implicit and explicit components of motor adaptation [18], and could plausibly explain the results of work reporting effects of cerebellar stimulation on motor savings [13], as recent research suggests savings may be linked to explicit learning mechanisms [19].…”

Sensitivity to Error During Visuomotor Adaptation is Similarly Modulated by Abrupt, Gradual and Random Perturbation Schedules

“…As an alternative account, savings has previously been explained by the retrieval of previous successful actions, reflecting the use of an explicit strategy (Avraham et al, 2021;Huang et al, 2011;Huberdeau et al, 2015;Morehead et al, 2015). Within the framework of a two-state model, this theory suggests that savings is driven purely by the fast process, without consideration of the contributions from the slow process.…”

“…The copyright holder for this preprint this version posted June 15, 2021. ; https://doi.org/10.1101/2021.06.14.448375 doi: bioRxiv preprint often relies on the use of verbal aiming reports prior to reaching (Avraham et al, 2021;Huberdeau et al, 2015;Morehead et al, 2015;Taylor et al, 2014). Recent findings, however, indicate that verbal aiming reports could lead to an overestimated explicit contribution to adaptation (de Brouwer et al, 2018;Leow et al, 2017).…”

“…Several researchers have argued that explicit cognitive strategies can account for a significant amount of learning, particularly during the early phase of learning and relearning (Mazzoni & Krakauer, 2006;Taylor et al, 2014;Taylor & Ivry, 2011). The dissociation of learning into implicit and explicit learning processes often relies on the use of verbal aiming reports prior to reaching (Avraham et al, 2021;Huberdeau et al, 2015;Morehead et al, 2015;Taylor et al, 2014). Recent findings, however, indicate that verbal aiming reports could lead to an overestimated explicit contribution to adaptation (de Brouwer et al, 2018;Leow et al, 2017).…”

“…The behavioural changes associated with savings suggest that some component of memory from the initial training must lead to the faster relearning, but what is remembered and recalled remains unclear (Avraham et al, 2021;Coltman et al, 2019;Herzfeld et al, 2014;Huang et al, 2011;Huberdeau et al, 2015;Leow et al, 2016Leow et al, , 2017Yin & Wei, 2020). One perspective argues for the enhancement of an explicit strategy (Avraham et al, 2021;Huberdeau et al, 2015;Morehead et al, 2015), while the other side suggests that faster relearning is driven by the experience of the motor errors (Coltman et al, 2019;Hanajima et al, 2015;Herzfeld et al, 2014;Leow et al, 2016).…”