The cerebellum does more than sensory prediction error-based learning in sensorimotor adaptation tasks

Abstract

Individuals with damage to the cerebellum perform poorly in sensorimotor adaptation paradigms. This deficit has been attributed to impairment in sensory prediction error-based updating of an internal forward model, a form of implicit learning. These individuals can, however, successfully counter a perturbation when instructed with an explicit aiming strategy. This successful use of an instructed aiming strategy presents a paradox: In adaptation tasks, why do individuals with cerebellar damage not come up with an aiming solution on their own to compensate for their implicit learning deficit? To explore this question, we employed a variant of a visuomotor rotation task in which, before executing a movement on each trial, the participants verbally reported their intended aiming location. Compared with healthy control participants, participants with spinocerebellar ataxia displayed impairments in both implicit learning and aiming. This was observed when the visuomotor rotation was introduced abruptly () or gradually (). This dual deficit does not appear to be related to the increased movement variance associated with ataxia: Healthy undergraduates showed little change in implicit learning or aiming when their movement feedback was artificially manipulated to produce similar levels of variability (). Taken together the results indicate that a consequence of cerebellar dysfunction is not only impaired sensory prediction error-based learning but also a difficulty in developing and/or maintaining an aiming solution in response to a visuomotor perturbation. We suggest that this dual deficit can be explained by the cerebellum forming part of a network that learns and maintains action-outcome associations across trials. Individuals with cerebellar pathology are impaired in sensorimotor adaptation. This deficit has been attributed to an impairment in error-based learning, specifically, from a deficit in using sensory prediction errors to update an internal model. Here we show that these individuals also have difficulty in discovering an aiming solution to overcome their adaptation deficit, suggesting a new role for the cerebellum in sensorimotor adaptation tasks.

Delineating cerebellar mechanisms in DYT11 myoclonus‐dystonia

“…Saccadic adaptation by contrast is a largely implicit task . The neural correlates of such task‐related differences are complex, but the cerebellum may be preferentially recruited with implicit paradigms that could therefore be important in driving the differences observed in DYT11 . Another alternative is that the saccadic adaptation deficits identify a cerebellar‐independent mechanism that is revealed selectively by testing saccadic adaptation .…”

“…10 The neural correlates of such task-related differences are complex, but the cerebellum may be preferentially recruited with implicit paradigms that could therefore be important in driving the differences observed in DYT11. 23,24 Another alternative is that the saccadic adaptation deficits identify a cerebellar-independent mechanism that is revealed selectively by testing saccadic adaptation. 10 Saccadic and limb adaptation are likely to involve overlapping distributed networks, but certain features such as brain stem processing are clearly more important in the control of eye movements.…”

Implicit visuomotor adaptation remains limited after several days of training

“…This was made possible by asking participants to report their intended aiming location (i.e. the direction that they intend to move in order to compensate for the perturbation), by verbally specifying a location relative to the target (Taylor et al, 2014, Bond andMcDougle et al 2015;Brudner et al 2016;McDougle et al 2017;Butcher et al 2017), or by tapping the surface of a touch screen Hutter and Taylor, 2018). In these experiments, participants reported their intended aiming location and then make a reaching movement.…”

The effects of awareness of the perturbation during motor adaptation on hand localization

“…Implicit components of adaptation are clearly independent of explicit components, differing both in the time course of their development during training (McDougle et al, 2015;Taylor et al, 2014) and in their development during the aging process (Heuer & Hegele, 2008). They are however related, as patients with cerebellar ataxia show deficits in both implicit and explicit aspects of reach adaptation (Butcher et al, 2017). We find that reach-aftereffects made without strategy were consistent regardless of instruction or the size of the perturbation.…”