Using gaze behavior to parcellate the explicit and implicit contributions to visuomotor learning

Abstract

Successful motor performance relies on our ability to adapt to changes in the environment by learning novel mappings between motor commands and sensory outcomes. Such adaptation is thought to involve two distinct mechanisms: an implicit, error-based component linked to slow learning and an explicit, strategic component linked to fast learning and savings (i.e., faster relearning). Because behavior, at any given moment, is the resultant combination of these two processes, it has remained a challenge to parcellate their relative contributions to performance. The explicit component to visuomotor rotation (VMR) learning has recently been measured by having participants verbally report their aiming strategy used to counteract the rotation. However, this procedure has been shown to magnify the explicit component. Here we tested whether task-specific eye movements, a natural component of reach planning, but poorly studied in motor learning tasks, can provide a direct readout of the state of the explicit component during VMR learning. We show, by placing targets on a visible ring and including a delay between target presentation and reach onset, that individual differences in gaze patterns during sensorimotor learning are linked to participants' rates of learning and their expression of savings. Specifically, we find that participants who, during reach planning, naturally fixate an aimpoint rotated away from the target location, show faster initial adaptation and readaptation 24 h later. Our results demonstrate that gaze behavior cannot only uniquely identify individuals who implement cognitive strategies during learning but also how their implementation is linked to differences in learning. NEW & NOTEWORTHY Although it is increasingly well appreciated that sensorimotor learning is driven by two separate components, an error-based process and a strategic process, it has remained a challenge to identify their relative contributions to performance. Here we demonstrate that task-specific eye movements provide a direct read-out of explicit strategies during sensorimotor learning in the presence of visual landmarks. We further show that individual differences in gaze behavior are linked to learning rate and savings.

Explicit feedback and instruction do not change shoulder muscle activity reduction after shoulder fixation

“…Reducing shoulder muscle activity after shoulder fixation with instruction and feedback Many previous studies have investigated the role of explicit cognitive strategies in motor learning de Brouwer et al 2018;Christou et al 2016;Mazzoni and Krakauer 2006;McDougle et al 2015;Miyamoto et al 2020;Poh et al 2016;Rand and Rentsch 2015;Stark-Inbar et al 2017; . Regardless of the type of learning studied (i.e., visuomotor rotation, forcefield, etc.…”

External error attribution dampens efferent-based predictions but not proprioceptive changes in hand localization

“…We ask people to make open-loop reaches to targets after adaptation, while either using the strategy they just learned (implicit and explicit), or not using it (only implicit). We use this measurement task as it doesn't seem to evoke additional explicit learning itself, as other methods do (Leow et al, 2017;de Brouwer et al, 2018;Maresch and Donchin, 2019), and to keep results comparable to earlier work from our lab (Modchalingam et al, 2019). While explicit learning does not necessarily lead to external error attribution, it is likely that external error attribution is accompanied with more explicit adaptation.…”

Implicit visuomotor adaptation remains limited after several days of training

“…The full effect of adaptation seen by Stratton (1896Stratton ( , 1897 and Kohler (1941Kohler ( , 1951aKohler ( , 1951b occurred following five full days of exposure. However, recent research has suggested that implicit adaptation remains stable over two days of training (de Brouwer et al, 2018;Huberdeau et al, 2019). This may be explained if it takes more than two days of exposure for fragile motor memories to transform into consolidated memories that are protected from disruption and more difficult to unlearn (Krakauer and Shadmehr, 2006;Criscimagna-Hemminger and Shadmehr, 2008; but see Caithness et al 2004).…”