Visuomotor Prediction Errors Modulate EEG Activity Over Parietal Cortex

Savoie, Félix-Antoine; Thénault, François; Whittingstall, Kevin; Bernier, Pierre‐Michel

doi:10.1038/s41598-018-30609-0

Cited by 40 publications

(47 citation statements)

References 107 publications

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“…As a matter of fact, the magnitude of postperturbation movement biases (Diedrichsen et al, 2005;Galea et al, 2015) is typically similar to the learning rate reported for implicit adaptation (Smith et al, 2006;McDougle et al, 2015). Interestingly, a recent electroencephalography (EEG) study has provided evidence that the parietal cortex may be involved in the directional reaching bias that emerges following single-trial exposure to a visuomotor rotation (Savoie et al, 2018). In that study, participants made reaching movements toward a visual target while being pseudorandomly exposed to a 45°visuomotor rotation (approximately every three trials).…”

Section: Introductionmentioning

confidence: 59%

“…One way to probe for implicit adaptation is to expose individuals to an intermittent or randomly changing perturbation and to investigate the directional movement bias that occurs on the following trial (Diedrichsen et al, 2005;Galea et al, 2015;Torrecillos et al, 2015;Tan et al, 2016;Savoie et al, 2018). Indeed, this bias has been suggested to be automatic and nonstrategic (Donchin et al, 2003;Galea et al, 2015), which arguably make it a valid proxy for implicit adaptation.…”

Section: Introductionmentioning

confidence: 99%

“…In light of the above, the goal of the present study was to test a causal relationship between the parietal responses observed by Savoie et al (2018) and the movement bias incurred by single-trial exposure to a visuomotor rotation. To do so, single-pulse transcranial magnetic stimulation (TMS) was used to disrupt either left or right parietal activity as participants were intermittently exposed to a 45°visuomotor rotation.…”

Section: Introductionmentioning

confidence: 99%

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Single-Pulse TMS over the Parietal Cortex Does Not Impair Sensorimotor Perturbation-Induced Changes in Motor Commands

Savoie

Dallaire-Jean

Thénault

et al. 2020

eNeuro

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Intermittent exposure to a sensorimotor perturbation, such as a visuomotor rotation, is known to cause a directional bias on the subsequent movement that opposes the previously experienced perturbation. To date, it is unclear whether the parietal cortex is causally involved in this postperturbation movement bias. In a recent electroencephalogram study, Savoie et al. (2018) observed increased parietal activity in response to an intermittent visuomotor perturbation, raising the possibility that the parietal cortex could subserve this change in motor behavior. The goal of the present study was to causally test this hypothesis. Human participants (N = 28) reached toward one of two visual targets located on either side of a fixation point, while being pseudorandomly submitted to a visuomotor rotation. On half of all rotation trials, single-pulse transcranial magnetic stimulation (TMS) was applied over the right (N = 14) or left (N = 14) parietal cortex 150 ms after visual feedback provision. To determine whether TMS influenced the postperturbation bias, reach direction was compared on trials that followed rotation with (RS 1 1) and without (R 1 1) TMS. It was hypothesized that interfering with parietal activity would reduce the movement bias following rotated trials. Results revealed a significant and robust postrotation directional bias compared with both rotation and null rotation trials. Contrary to our hypothesis, however, neither left nor right parietal stimulation significantly impacted the postrotation bias. These data suggest that the parietal areas targeted here may not be critical for perturbation-induced motor output changes to emerge.

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Section: Introductionmentioning

confidence: 59%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Single-Pulse TMS over the Parietal Cortex Does Not Impair Sensorimotor Perturbation-Induced Changes in Motor Commands

Savoie

Dallaire-Jean

Thénault

et al. 2020

eNeuro

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“…From a neurophysiological standpoint, the posterior parietal cortex (PPC) is often considered to be a key structure both for eye-hand coordination (Dean et al 2012;Hwang et al 2014;Van Donkelaar et al 2000) and for adaptation to visuomotor rotation (Haar et al 2015;Mutha et al 2011;Savoie et al 2018). Many neurons in PPC are influenced by both eye and hand actions (Carey 2000).…”

Section: Separate Contribution Of Eye Movements To Hand Tracking and mentioning

confidence: 99%

Eye movements do not play an important role in the adaptation of hand tracking to a visuomotor rotation

Gouirand

Mathew

Brenner

et al. 2019

Journal of Neurophysiology

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Gouirand N, Mathew J, Brenner E, Danion FR. Eye movements do not play an important role in the adaptation of hand tracking to a visuomotor rotation. Adapting hand movements to changes in our body or the environment is essential for skilled motor behavior. Although eye movements are known to assist hand movement control, how eye movements might contribute to the adaptation of hand movements remains largely unexplored. To determine to what extent eye movements contribute to visuomotor adaptation of hand tracking, participants were asked to track a visual target that followed an unpredictable trajectory with a cursor using a joystick. During blocks of trials, participants were either allowed to look wherever they liked or required to fixate a cross at the center of the screen. Eye movements were tracked to ensure gaze fixation as well as to examine free gaze behavior. The cursor initially responded normally to the joystick, but after several trials, the direction in which it responded was rotated by 90°. Although fixating the eyes had a detrimental influence on hand tracking performance, participants exhibited a rather similar time course of adaptation to rotated visual feedback in the gaze-fixed and gaze-free conditions. More importantly, there was extensive transfer of adaptation between the gazefixed and gaze-free conditions. We conclude that although eye movements are relevant for the online control of hand tracking, they do not play an important role in the visuomotor adaptation of such tracking. These results suggest that participants do not adapt by changing the mapping between eye and hand movements, but rather by changing the mapping between hand movements and the cursor's motion independently of eye movements.NEW & NOTEWORTHY Eye movements assist hand movements in everyday activities, but their contribution to visuomotor adaptation remains largely unknown. We compared adaptation of hand tracking under free gaze and fixed gaze. Although our results confirm that following the target with the eyes increases the accuracy of hand movements, they unexpectedly demonstrate that gaze fixation does not hinder adaptation. These results suggest that eye movements have distinct contributions for online control and visuomotor adaptation of hand movements.

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“…It has been proposed that the 75 P300 reflects the updating of a model of stimulus context (Donchin and Coles 1988). Both the FRN 76 and the P300 have been observed in response to errors in motor tasks (Krigolson et al 2008; Torrecil-77 los et al 2014;MacLean et al 2015;Reuter et al 2018;Savoie et al 2018) . In this paper we describe 78 experiments in which we isolated and compared EEG responses to both reward and sensory error 79 feedback using separate adaptation paradigms that produced comparable changes in behavior.…”

mentioning

confidence: 99%

Neural Signatures of Reward and Sensory Prediction Error in Motor Learning

Cashaback

Gribble

2018

Preprint

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22Two distinct processes contribute to changes in motor commands during reach adaptation: 23 reward based learning and sensory error based learning. In sensory error based learning, the 24 mapping between sensory targets and motor commands is recalibrated according to error 25 feedback. In reward based learning, motor commands are associated with subjective value, 26 such that successful actions are reinforced. We recorded EEG from humans of either sex to 27 identify and dissociate the neural correlates of reward prediction error (RPE) and sensory 28 prediction error (SPE) during learning tasks designed to isolate each response. We designed a 29 visuomotor rotation task to isolate sensory error based learning in response to SPE, which was 30 induced by altered visuospatial feedback of hand position. In a reward learning task, we 31 isolated learning in response to RPE, which was induced by binary reward feedback. We found 32 that a fronto-central event related potential called the feedback related negativity occurred 33 specifically in response to RPE during reward based learning, while a more posterior component 34 called the P300 was associated with SPE during a visuomotor rotation task. These findings 35 reveal a dissociation between well characterized EEG signatures of error processing in two 36 distinct motor learning processes. CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/262576 doi: bioRxiv preprint first posted online Feb. 9, 2018; Page 3 Significance Statement 44Adaptation of motor output to changing task demands and dynamic environments is thought to 45 occur on the basis of distinct forms of prediction error. Reward prediction error occurs when 46 the subjective value of an outcome is different than the expected value, while sensory 47 prediction error occurs when the low-level sensory consequences of motor commands are 48 different than predicted. It remains unclear how EEG activity patterns associated with error 49 processing apply to these distinct forms of motor adaptation. We found that an event related 50 potential component called the feedback related negativity responded only to reward 51 prediction error, while the P300 component is modulated by sensory prediction error and 52 correlated to sensory error based learning.

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Visuomotor Prediction Errors Modulate EEG Activity Over Parietal Cortex

Cited by 40 publications

References 107 publications

Single-Pulse TMS over the Parietal Cortex Does Not Impair Sensorimotor Perturbation-Induced Changes in Motor Commands

Single-Pulse TMS over the Parietal Cortex Does Not Impair Sensorimotor Perturbation-Induced Changes in Motor Commands

Eye movements do not play an important role in the adaptation of hand tracking to a visuomotor rotation

Neural Signatures of Reward and Sensory Prediction Error in Motor Learning

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