Cerebellar anodal tDCS increases implicit visuomotor remapping when strategic re-aiming is suppressed

The cerebellum is known to be 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, 24 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. This suggests that cerebellar anodal tDCS increased implicit remapping during sensorimotor adaptation irrespective of preparation time constraints. This work shows that the cerebellum is critical in the formation of new visuomotor maps that correct perturbations in sensory feedback, both when explicit processes are suppressed and when allowed during sensorimotor adaptation.


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function alter behaviour when compensating for sensorimotor perturbations, as shown by non-invasive 22 stimulation of the cerebellum and studies involving patients with cerebellar degeneration. It is known, 23 however, that behavioural responses to sensorimotor perturbations reflect both explicit processes (such as 24 volitional aiming to one side of a target to counteract a rotation of visual feedback) and implicit, error-25 driven updating of sensorimotor maps. The contribution of the cerebellum to these explicit and implicit 26 processes remains unclear. Here, we examined the role of the cerebellum in sensorimotor adaptation to a 27 30° rotation of visual feedback of hand position during target-reaching, when the capacity to use explicit 28 processes was manipulated by controlling movement preparation times. Explicit re-aiming was 29 suppressed in one condition by requiring subjects to initiate their movements within 300ms of target 30 presentation, and permitted in another condition by requiring subjects to wait approximately 1050ms after 31 target presentation before movement initiation. Similar to previous work, applying anodal transcranial 32 direct current stimulation (tDCS; 1.5mA) to the right cerebellum during adaptation resulted in faster 33 compensation for errors imposed by the rotation. After exposure to the rotation, we evaluated implicit 34 remapping in no-feedback trials after providing participants with explicit knowledge that the rotation had 35 been removed. Crucially, movements were more adapted in these no-feedback trials following cerebellar 36 anodal tDCS than after sham stimulation in both long and short preparation groups. This suggests that 37 cerebellar anodal tDCS increased implicit remapping during sensorimotor adaptation irrespective of The cerebellum has long been known to play a crucial role in predicting the sensory consequences of 45 motor commands [1]; a process that appears necessary both for rapid online responses to unexpected 46 events, and for trial-by-trial compensation of systematic sensorimotor disturbances (for recent reviews, 47 see [2, 3]). When a perturbation of sensory feedback (e.g., a rotation in visual feedback of a movement 48 trajectory, or a force field that pushes the moving hand away from its intended direction) evokes a 49 mismatch between the predicted sensory outcomes and the actual sensory outcomes, the internal mapping 50 between motor commands and resulting changes in sensory state is thought to be updated, such that the 51 prediction error is minimized in subsequent movements. The likely involvement of the cerebellum in this 52 process is supported by a large body of computational, neurophysiological and neuropsychological work.

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Participants made centre-out horizontal reaching movements by moving the handle of the manipulandum 120 to move an on-screen circular cursor (radius 0.25cm) from a start circle (radius 0.5cm) to a target circle 121 (radius 0.5cm), projected on a computer monitor (ASUS, VG278H, Taiwan) running at 60Hz mounted 122 above the vBOT via a mirror in a darkened room. Participants observed the monitor via its reflection onto 123 a horizontal mirror which prevented direct vision of their arm, and gave the illusion that the cursor and 124 targets were located in the plane of hand motion. Participants were seated on a chair height-adjusted to 125 allow optimal viewing of the screen for the duration of the experiment. The right forearm was supported 126 by an air-sled which rested on a glass table. Compressed air was forced out of small holes in the air-sled 127 runners, which allowed low friction in the plane of movement. Targets appeared randomly in one of eight 128 locations (0°, 45°, 90°, 135°, 180°, 225°, 270° and 315° relative to the start circle located centrally on-129 screen). The distance from the center of the start circle to the center of the targets was 9cm.

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Participants were instructed that their goal was to move the cursor (radius 0.25cm) as accurately as 132 possible from the start circle (radius 0.5 cm) to the target circle (radius 0.5cm). Participants were 133 instructed not to stop on the target, but to slice through the target. Across all conditions, a sequence of 134 three tones spaced 500 ms apart were presented at a clearly audible volume via external speakers.

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In addition, to examine the rate of adaptation without the possible confound of intrinsic bias in movement 187 direction, we also fit cycle-averaged movement directions for each dataset to a single-rate exponential 188 function [39], as follows: where y is the movement direction, x is the trial number, k is the rate constant that indicates the rate with 190 which movement direction changes, a is the movement direction at which performance reaches 191 asymptote, and y 0 + a is the hypothetical y value when x is zero.

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We also examined the rate of de-adaptation in the washout block by fitting cycle-averaged movement

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Early adaptation: After the 30° rotation was imposed, participants compensated for the error 240 imposed by the rotation by moving in the opposite direction to the rotation (see Figure 1 Figure 3A). Rate constants for the groups receiving anodal tDCS tended to be larger than rate 277 constants for the groups receiving sham tDCS (see Figure 3A).

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We also found that increasing cerebellar excitability with anodal tDCS increased the rate at which 358 participants altered movements to (1) reduce errors resulting from a rotation in the adaptation phase, and

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(2) reduce errors resulting from sudden removal of a rotation after adapting movements to the rotation.  Previous work using non-invasive brain stimulation demonstrated that the cerebellum plays a role in 412 sensorimotor adaptation, however, because these studies did not dissociate explicit and implicit processes 413 that occur during adaptation, it was unclear whether the cerebellum plays a role in implicit or explicit 414 processes, or both. Here, we show that when explicit re-aiming processes is suppressed, increasing 415 cerebellar excitability via anodal tDCS increases implicit remapping after adaptation to a 30° rotation.

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Thus, the cerebellum contributes to implicit sensorimotor remapping when people learn to compensate a 417 visuomotor rotation. 418 419 420