Cerebellar anodal tDCS increases implicit learning when strategic re-aiming is suppressed in sensorimotor adaptation

Abstract

Neurophysiological and neuroimaging work suggests that the cerebellum is critically involved in sensorimotor adaptation. Changes in cerebellar function alter behaviour when compensating for sensorimotor perturbations, as shown by non-invasive stimulation of the cerebellum and studies involving patients with cerebellar degeneration. It is known, however, that behavioural responses to sensorimotor perturbations reflect both explicit processes (such as volitional aiming to one side of a target to counteract a rotation of visual feedback) and implicit, error-driven updating of sensorimotor maps. The contribution of the cerebellum to these explicit and implicit processes remains unclear. Here, we examined the role of the cerebellum in sensorimotor adaptation to a 30° rotation of visual feedback of hand position during target-reaching, when the capacity to use explicit processes was manipulated by controlling movement preparation times. Explicit re-aiming was suppressed in one condition by requiring subjects to initiate their movements within 300ms of target presentation, and permitted in another condition by requiring subjects to wait approximately 1050ms after target presentation before movement initiation. Similar to previous work, applying anodal transcranial direct current stimulation (tDCS; 1.5mA) to the right cerebellum during adaptation resulted in faster compensation for errors imposed by the rotation. After exposure to the rotation, we evaluated implicit remapping in no-feedback trials after providing participants with explicit knowledge that the rotation had been removed. Crucially, movements were more adapted in these no-feedback trials following cerebellar anodal tDCS than after sham stimulation in both long and short preparation groups. Thus, cerebellar anodal tDCS increased implicit remapping during sensorimotor adaptation, irrespective of preparation time constraints. The results are consistent with the possibility that the cerebellum contributes to the formation of new visuomotor maps that correct perturbations in sensory feedback, even when explicit processes are suppressed during sensorimotor adaptation.

Neural changes associated with cerebellar tDCS studied using MR spectroscopy

“…Although participants showed a clear ability to adapt to the novel visuomotor rotation, the expected significant enhancement of adaptation by anodal cerebellar tDCS, that had been shown in various studies (Galea et al 2011 ; Hardwick and Celnik 2014 ; Block and Celnik 2013 ; Leow et al 2017 ), was not observed here. Despite our sample size being in the same range of previously published tDCS papers, a recent study indicates this could be significantly under powered (Minarik et al 2016 ).…”

“…For instance, Galea et al ( 2011 ) applied anodal cerebellar tDCS during visuomotor adaptation and found anodal cerebellar tDCS led to faster adaptation, relative to either primary motor cortex (M1) anodal tDCS or sham tDCS (Galea et al 2011 ). This effect on motor adaptation/learning has been replicated in visuomotor adaptation (Hardwick and Celnik 2014 ; Block and Celnik 2013 ; Doppelmayr et al 2016 ; Leow et al 2017 ), force-field adaptation (Herzfeld et al 2014 ), locomotor adaptation (Jayaram et al 2012 ), saccade adaptation (Panouilleres et al 2015 ; Avila et al 2015 ), motor skill learning (Cantarero et al 2015 ), and language prediction tasks (Miall et al 2016 ). As a result, it has been suggested that cerebellar tDCS is not only a useful tool to understand cerebellar function but also as a possible clinical technique to restore cerebellar function in patients suffering from cerebellar-based disorders (Grimaldi et al 2014 ).…”

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.…”

Of hands, tools, and exploding dots: How different action states and effects separate visuomotor memories

“…Notably, limiting standard implicit adaptation to a body model does not necessarily contradict the idea that internal models and the cerebellum underlie tool transformations (Imamizu et al 2003;Higuchi et al 2007;Imamizu and Kawato 2009). Recent neuroimaging and patient studies indicate that cerebellum-based internal models support not only the implicit (Leow et al 2017), but also the explicit component of visuomotor adaptation (Werner et al 2014;Butcher et al 2017). A possibility is that internal models support the selection of suitable actions by simulating their hypothetical outcomes (Barsalou 1999).…”