Neural correlates of adaptation to gradual and to sudden visuomotor distortions in humans

Abstract

This study aimed at scrutinizing the neural correlates of sensorimotor adaptation. Subjects were exposed either to a gradually (group G) or to a suddenly introduced perturbation (group S) followed by a test of aftereffects. They were also exposed to a control condition equated for their movement errors during the adaptation condition. We registered subjects' brain activity by functional magnetic resonance imaging. Behavioral data revealed no difference between aftereffects in G and S, while imaging data suggest different neural correlates. Direct comparison between groups showed more adaptation-related activation in left cingulate and inferior frontal as well as right caudate and temporal areas in S than in G. In contrast, no neural activity was related more to G than to S and no common activations were found for both groups. Within-group analyses further revealed right inferior parietal lobe, cerebellar and cingulate cortex activity in group S and activation of frontal lobe and left cerebellum in group G for a contrast between adaptation condition and baseline. Less brain activity was observed when controlled for movement errors: the contrast between adaptation and control condition yielded left occipital lobe activity in group S, and left posterior dentate nucleus and brainstem activity in group G. The present data confirm an involvement of the cerebellar cortex in error processing during sudden adaptation, since this activation was found for the contrast 'adaptation-baseline' but not for 'adaptation-control.' In addition, our data suggest an involvement of deep cerebellar nuclei in the adaptation to gradually introduced distortions.

Intermanual transfer of visuomotor adaptation is related to awareness

“…Compared to sudden adaptation, performance in aftereffect tests was previously shown to be improved after gradual saccade [37] and prism adaptation [1], after gradual adaptation to a visual gain [38] and to a 90 deg rotation [39]. Adaptation to smaller visual rotations (30 deg and 60 deg), however, did not lead to a difference of aftereffects between gradual or sudden adaptation [34,40]. This is in line with the present findings.…”

Formation of model-free motor memories during motor adaptation depends on perturbation schedule

“…The existence of savings is another way of assessing the transfer of motor memories. Therefore, the absence of faster relearning between initial gradual learning and ensuing abrupt adaptation (i.e., limited transfer) suggests that gradual and abrupt schedules give rise to two different motor memories, which rely on largely nonoverlapping neural representations (Orban de Xivry et al 2011Werner et al 2014). This implies that the behavioral differences observed after abrupt and gradual adaptation to a perturbation (Abeele and Bock 2001;Berniker and Körding 2008;Buch et al 2003;Habagishi et al 2014;Kagerer et al 1997;Klassen et al 2005;Kluzik et al 2008;Michel et al 2007;Saijo and Gomi 2010;TorresOviedo and Bastian 2012;Wong and Shelhamer 2011) do not stem from a single motor memory that acquires different features depending on the schedule but from different memories, with different neural representations and hence different features.…”

Explicit strategies in force field adaptation

“…In this manuscript, we have tended to contrast adaptation of internal models with explicit strategies. While we indeed believe that explicit strategies are qualitatively distinct from canonical adaptation of internal models and rely on different neural substrates (Anguera et al 2010(Anguera et al , 2012Werner et al 2014;Thürer et al 2016), we would like to emphasize that this does not mean that explicit strategies do not rely on internal models or the cerebellum (Butcher et al 2017). Internal models may serve various purposes, such as simulating potential outcomes to support (explicit) action selection (Barsalou 1999) and further research is needed to understand these relations.…”

“…For the same reasons, all of our experiments used only a single target direction, as this reduces the participants' experience of the force field to mainly the horizontal component. Furthermore, we used rather large field constants in experiment 3; lower field constants would likely spur less explicit learning, similar to the way smaller or gradually introduced cursor rotations do (Malfait and Ostry 2004;Kagerer et al 2006;Werner et al 2014;Gaffin-Cahn et al 2019). It therefore seems likely that the explicit component plays less of a role in force field paradigms that use small field constants, multiple targets, and deliberately instruct their participants to "not think about the task" (Morehead et al 2017).…”