Formation of a long-term memory for visuomotor adaptation following only a few trials of practice

Huberdeau, David; Haith, Adrian M.; Krakauer, John W.

doi:10.1152/jn.00369.2015

Cited by 99 publications

(104 citation statements)

References 69 publications

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“…Patients and older controls also exhibited savings (larger performance gains in the first 4 cycles after rotation onset) in Bout 3 compared to Bout 2 (patients: z = -2.09, p = 0.07; controls: z = -2.46, p = 0.03) but not between Bouts 1 and 2 (patients: z = 1.12, p = 0.26; controls: z = 0.80, p = 0.42). This savings without an accompanying performance improvement in Bout 3 suggests that the learned aiming direction in Bout 2 was simply retrieved in Bout 3, consistent with previous work attributing savings to recall of an aiming strategy Huberdeau et al, 2015a;Morehead et al, 2015).…”

Section: Vision Of the Hand Modified Performance In Response To A Vissupporting

confidence: 86%

Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?

Wong

Marvel

Taylor

et al. 2018

Preprint

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Systematic perturbations in motor adaptation tasks are primarily countered by learning from sensory-prediction errors, with secondary contributions from other learning processes.Despite the availability of these additional processes, particularly the use of explicit re-aiming to counteract observed target errors, patients with cerebellar degeneration are surprisingly unable to compensate for their sensory-prediction-error deficits by spontaneously switching to another learning mechanism. We hypothesized that if the nature of the task was changedby allowing vision of the hand, which eliminates sensory-prediction errorspatients could be induced to preferentially adopt aiming strategies to solve visuomotor rotations. To test this, we first developed a novel visuomotor rotation paradigm that provides participants with vision of their hand in addition to the cursor, effectively setting the sensory-prediction-error signal to zero. We demonstrated in younger healthy controls that this promotes a switch to strategic re-aiming based on target errors. We then showed that with vision of the hand, patients with spinocerebellar ataxia could also switch to an aiming strategy in response to visuomotor rotations, performing similarly to age-matched participants (older controls). Moreover, patients could retrieve their learned aiming solution after vision of the hand was removed, and retain it for at least one year.Both patients and older controls, however, exhibited impaired overall adaptation performance compared to younger healthy controls (age, 18-33), likely due to age-related reductions in spatial and working memory. Moreover, patients failed to generalize, i.e., they were unable to adopt analogous aiming strategies in response to novel rotations, nor could they further improve their performance without vision of the hand. Hence, there appears to be an inescapable obligatory dependence on sensory-prediction-error-based learningeven when this system is impaired in patients with cerebellar degeneration. The persistence of sensory-prediction-error-based learning 3 effectively suppresses a switch to target-error-based learning, which perhaps explains the unexpectedly poor performance by patients with spinocerebellar ataxia in visuomotor adaptation tasks.

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Section: Vision Of the Hand Modified Performance In Response To A Vissupporting

confidence: 86%

Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?

Wong

Marvel

Taylor

et al. 2018

Preprint

Self Cite

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“…Task errors that 635 could not be corrected (i.e., enforced task errors that occurred regardless of the 636 participants' behaviour) did not improve learning. Furthermore, Experiment 2 showed 637 that task errors need not be present upon re-exposure to the perturbation, 638 contradicting the proposal that task errors act as a retrieval cue to trigger savings 639 (Huberdeau et al, 2015a). 640 with a non-obligatory expression of the learning, because we can choose to achieve 674 behavioural goals in many different ways.…”

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confidence: 95%

“…A few 380 interpretations are possible. First, task errors might act as a retrieval cue to trigger 381 the memory that is responsible for savings (Huberdeau et al, 2015a). Second, task 382 errors might be necessary to encode a memory that is responsible for savings.…”

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confidence: 99%

Task errors drive memories that improve sensorimotor adaptation

Leow

Marinovic

Rugy

et al. 2019

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11Traditional views of sensorimotor adaptation, or adaptation of movements to 12 perturbed sensory feedback, emphasize the role of automatic, implicit correction of 13 sensory prediction errors (differences between predicted and actual sensory 14 outcomes). However, latent memories formed from sensorimotor adaptation, 15 prominently evidenced in improved learning (i.e., savings), have recently been 16 attributed to strategic corrections of task errors (failures to achieve task goals). To 17 dissociate contributions of task errors and sensory prediction errors to latent 18 sensorimotor memories, we perturbed target locations to remove or enforce task 19 errors during learning and/or test. We show that prior learning to correct task errors 20 was sufficient for savings: a history of sensory prediction errors was neither sufficient 21 nor obligatory for savings. Limiting movement preparation time further revealed two 22 distinct components of this learning: 1) time-consuming, flexible strategies, and 2) 23 rapidly expressible, inflexible stimulus-response associations. The results show that 24 adaptive responses to sensorimotor perturbations take many forms. Herzfeld et al., 2014). According to this idea, experiencing a 66 systematic sequence of errors generates a memory of errors, which increases 67 sensitivity to those errors and the gain of error correction when reencountering 68 similar errors (Gonzalez Castro et al., 2014; Herzfeld et al., 2014). 65 Castro 69Despite the importance of the phenomenon of savings for the broad field of 70 3 motor learning, interest in the processes that underlie the effect has declined since 71 the emergence of compelling evidence that savings in standard visuomotor rotation 72 tasks is dominated by volitional, strategic selection of actions that restore task 73 success (Avraham et al., 2019; de Brouwer et al., 2017; Haith et al., 2015; Morehead 74 et al., 2015). For example, if leftward displacement of visual feedback causes a 75 person to miss the target to the left, they tend to deliberately aim to the right of the 76 target to counteract the error (Uhlarik, 1973). Using cues to signal perturbation onset 77 prompted rapid re-selection of the adapted movement on the first trial, even before 78 participants re-experienced the previously encountered error (Morehead et al., 79 2015). Similarly, suppressing strategy use by limiting movement preparation time 80 prevented the expression of savings (Haith et al., 2015). If savings were solely a 81 manifestation of deliberate strategy use, then "cognitive" functions which determine 82 how successfully one might acquire and implement strategies would be central to 83 acquisition of latent sensorimotor memories: non-strategic "motor" processes would 84 thus be of less importance. 85 But is the conscious awareness of a strategy, to apply a corrective movement 86 that already exists within the participant's motor repertoire, really all that is retained 87 when a person adapts movement to a perturbation? Or are there components of ...

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“…Moreover, the motor adaptation process was not complete as summed error did not fully return to that of late familiarization, so it is not possible to measure how/if IMC would have developed further or how/if IMC would have decreased in parallel with the full decrease of error and of learning itself. It would be interesting to test whether changes in IMC become substantiated and robust in longer term motor adaptation protocols and follow the “savings” measured in follow-up adaptation sessions on future days/weeks (Haith et al, 2015; Huberdeau et al, 2015). Evidence of high frequency activity may give crucial physiological insight into mechanisms of functional recovery and, following the examples found in the literature (Nishimura et al, 2009; Kisiel-Sajewicz et al, 2011; Fisher et al, 2012; Bravo-Esteban et al, 2014), we suggest high frequency IMC (40–100 Hz) should be further investigated in long term neurological conditions such as stroke.…”

Section: Discussionmentioning

confidence: 99%

High-Frequency Intermuscular Coherence between Arm Muscles during Robot-Mediated Motor Adaptation

et al. 2017

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Adaptation of arm reaching in a novel force field involves co-contraction of upper limb muscles, but it is not known how the co-ordination of multiple muscle activation is orchestrated. We have used intermuscular coherence (IMC) to test whether a coherent intermuscular coupling between muscle pairs is responsible for novel patterns of activation during adaptation of reaching in a force field. Subjects (N = 16) performed reaching trials during a null force field, then during a velocity-dependent force field and then again during a null force field. Reaching trajectory error increased during early adaptation to the force-field and subsequently decreased during later adaptation. Co-contraction in the majority of all possible muscle pairs also increased during early adaptation and decreased during later adaptation. In contrast, IMC increased during later adaptation and only in a subset of muscle pairs. IMC consistently occurred in frequencies between ~40–100 Hz and during the period of arm movement, suggesting that a coherent intermuscular coupling between those muscles contributing to adaptation enable a reduction in wasteful co-contraction and energetic cost during reaching.

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Formation of a long-term memory for visuomotor adaptation following only a few trials of practice

Abstract: Huberdeau DM, Haith AM, Krakauer JW. Formation of a long-term memory for visuomotor adaptation following only a few trials of practice.

Cited by 99 publications

References 69 publications

Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?

Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?

Task errors drive memories that improve sensorimotor adaptation

High-Frequency Intermuscular Coherence between Arm Muscles during Robot-Mediated Motor Adaptation

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