The Consolidation of Newly Learned Movements Depends upon the Somatosensory Cortex in Humans.

Studies using magnetic brain stimulation indicate the involvement of somatosensory regions in the acquisition and retention of newly learned movements. Recent work found an impairment in motor memory when retention was tested shortly after the application of continuous theta-burst stimulation (cTBS) to the primary somatosensory cortex, compared with stimulation of the primary motor cortex or a control zone. This finding that the somatosensory cortex is involved in motor memory retention whereas the motor cortex is not, if confirmed, could alter our understanding of human motor learning. It would indicate that plasticity in sensory systems underlies newly learned movements, which is different than the commonly held view that adaptation learning involves updates to a motor controller. Here we test this idea. Participants were trained in a visuomotor adaptation task, with visual feedback gradually shifted. Following adaptation, cTBS was applied either to M1, S1, or an occipital cortex control area. Participants were tested for retention 24 h later. It was observed that S1 stimulation led to reduced retention of prior learning, compared with stimulation of M1 or the control area (with no significant difference between M1 and control). In a further control, cTBS was applied to S1 following training with unrotated feedback, in which no learning occurred. This had no effect on movement in the retention test indicating the effects of S1 stimulation on movement are learning specific. The findings are consistent with the S1 participation in the encoding of learning-related changes to movements and in the retention of human motor memory.

Imprecise perception of hand position during early motor adaptation.

Localizing one's body parts is important for movement control and motor learning. Recent studies have shown that the precision with which people localize their hand places constraints on motor adaptation. Although these studies have assumed that hand localization remains equally precise across learning, we show that precision decreases rapidly during early motor learning. In three experiments, healthy young participants (n = 92) repeatedly adapted to a 45° visuomotor rotation for a cycle of two to four reaches, followed by a cycle of two to four reaches with veridical feedback. Participants either used an aiming strategy that fully compensated for the rotation (experiment 1), or always aimed directly at the target, so that adaptation was implicit (experiment 2). We omitted visual feedback for the last reach of each cycle, after which participants localized their unseen hand. We observed an increase in the variability of angular localization errors when subjects used a strategy to counter the visuomotor rotation (experiment 1). This decrease in precision was less pronounced in the absence of reaiming (experiment 2), and when subjects knew that they would have to localize their hand on the upcoming trial, and could thus focus on hand position (experiment 3). We propose that strategic reaiming decreases the precision of perceived hand position, possibly due to attention to vision rather than proprioception. We discuss how these dynamics in precision during early motor learning could impact on motor control and shape the interplay between implicit and strategy-based motor adaptation.NEW & NOTEWORTHY Recent studies indicate that the precision with which people localize their hand limits implicit visuomotor learning. We found that localization precision is not static, but decreases early during learning. This decrease is pronounced when people apply a reaiming strategy to compensate for a visuomotor perturbation and is partly resistant to allocation of attention to the hand. We propose that these dynamics in position sense during learning may influence how implicit and strategy-based motor adaption interact.

Cerebellar GABA Change during Visuomotor Adaptation Relates to Adaptation Performance and Cerebellar Network Connectivity: A Magnetic Resonance Spectroscopic Imaging Study.

Motor adaptation is crucial for performing accurate movements in a changing environment and relies on the cerebellum. Although cerebellar involvement has been well characterized, the neurochemical changes in the cerebellum underpinning human motor adaptation remain unknown. We used a novel magnetic resonance spectroscopic imaging (MRSI) technique to measure changes in the inhibitory neurotransmitter GABA in the human cerebellum during visuomotor adaptation. Participants (n = 17, six female) used their right hand to adapt to a rotated cursor in the scanner, compared with a control task requiring no adaptation. We spatially resolved adaptation-driven GABA changes at the cerebellar nuclei and cerebellar cortex in the left and the right cerebellar hemisphere independently and found that simple right-hand movements increase GABA in the right cerebellar nuclei and decreases GABA in the left. When isolating adaptation-driven GABA changes, we found that GABA in the left cerebellar nuclei and the right cerebellar nuclei diverged, although GABA change from baseline at the right cerebellar nuclei was not different from zero at the group level. Early adaptation-driven GABA fluctuations in the right cerebellar nuclei correlated with adaptation performance. Participants showing greater GABA decrease adapted better, suggesting early GABA change is behaviorally relevant. Early GABA change also correlated with functional connectivity change in a cerebellar network. Participants showing greater decreases in GABA showed greater strength increases in cerebellar network connectivity. Results were specific to GABA, to adaptation, and to the cerebellar network. This study provides first evidence for plastic changes in cerebellar neurochemistry during motor adaptation. Characterizing these naturally occurring neurochemical changes may provide a basis for developing therapeutic interventions to facilitate human motor adaptation.SIGNIFICANCE STATEMENT Despite motor adaptation being fundamental to maintaining accurate movements, its neurochemical basis remains poorly understood, perhaps because measuring neurochemicals in the human cerebellum is technically challenging. Using a novel magnetic resonance spectroscopic imaging method, this study provides evidence for GABA changes in the left compared with the right cerebellar nuclei driven by both simple movement and motor adaptation. Although right cerebellar GABA changes were not significantly different from zero at the group level, the adaptation-driven GABA fluctuations in the right cerebellar nuclei correlated with adaptation performance and with functional connectivity change in a cerebellar network. These results show the first evidence for plastic changes in cerebellar neurochemistry during a cerebellar learning task. This provides the basis for developing therapeutic interventions that facilitate these naturally occurring changes to amplify cerebellar-dependent learning.

EEG responses induced by cerebellar TMS at rest and during visuomotor adaptation.

BACKGROUND: Connections between the cerebellum and the cortex play a critical role in learning and executing complex behaviours. Dual-coil transcranial magnetic stimulation (TMS) can be used non-invasively to probe connectivity changes between the lateral cerebellum and motor cortex (M1) using the motor evoked potential as an outcome measure (cerebellar-brain inhibition, CBI). However, it gives no information about cerebellar connections to other parts of cortex. OBJECTIVES: We used electroencephalography (EEG) to investigate whether it was possible to detect activity evoked in any areas of cortex by single-pulse TMS of the cerebellum (cerebellar TMS evoked potentials, cbTEPs). A second experiment tested if these responses were influenced by the performance of a cerebellar-dependent motor learning paradigm. METHODS: In the first series of experiments, TMS was applied over either the right or left cerebellar cortex, and scalp EEG was recorded simultaneously. Control conditions that mimicked auditory and somatosensory inputs associated with cerebellar TMS were included to identify responses due to non-cerebellar sensory stimulation. We conducted a follow-up experiment that evaluated whether cbTEPs are behaviourally sensitive by assessing individuals before and after learning a visuomotor reach adaptation task. RESULTS: A TMS pulse over the lateral cerebellum evoked EEG responses that could be distinguished from those caused by auditory and sensory artefacts. Significant positive (P80) and negative peaks (N110) over the contralateral frontal cerebral area were identified with a mirrored scalp distribution after left vs. right cerebellar stimulation. The P80 and N110 peaks were replicated in the cerebellar motor learning experiment and changed amplitude at different stages of learning. The change in amplitude of the P80 peak was associated with the degree of learning that individuals retained following adaptation. Due to overlap with sensory responses, the N110 should be interpreted with caution. CONCLUSIONS: Cerebral potentials evoked by TMS of the lateral cerebellum provide a neurophysiological probe of cerebellar function that complements the existing CBI method. They may provide novel insight into mechanisms of visuomotor adaptation and other cognitive processes.

Signatures of contextual interference in implicit sensorimotor adaptation.

Contextual interference refers to the phenomenon whereby a blocked practice schedule results in faster acquisition but poorer retention of new motor skills compared to a random practice schedule. While contextual interference has been observed under a broad range of tasks, it remains unclear if this effect generalizes to the implicit and automatic recalibration of an overlearned motor skill. To address this question, we compared blocked and random practice schedules in a visuomotor rotation task that isolates implicit adaptation. In experiment 1, we found robust signatures of contextual interference in implicit adaptation: compared to participants tested under a blocked training schedule, participants tested under a random training schedule exhibited a reduced rate of learning during the training phase but better retention during a subsequent no-feedback assessment phase. In experiment 2, we again observed an advantage in retention following random practice and showed that this result was not due to a change in context between the training and assessment phases (e.g. a blocked training schedule followed by a random assessment schedule). Taken together, these results indicate that contextual interference is not limited to the acquisition of new motor skills but also applies to the implicit adaptation of established motor skills.

The influence of learning history on anterograde interference.

Classically interpreted as a competition between opposite memories (A vs B), anterograde interference (AI) also emerges in the absence of competing memories (A vs A), suggesting that mechanisms other than those involved in memory competition contribute to AI. To investigate this, we tested the hypothesis that extending motor practice would enhance a first memory, but come at the cost of reduced learning capabilities when subsequently exposed to a second learning session of the same task. Based on converging biological evidence, AI was expected to depend upon the degree of extended practice of the initial exposure. During a first Session, four conditions were carried out where participants (n = 24) adapted to a gradually introduced -20° visual deviation while the extent of the initial exposure was manipulated by varying the duration or type of the performance asymptote. Specifically, the performance asymptote at -20° was either Short (40 trials), Moderate (160 trials), Long (320 trials), or absent due to continuously changing perturbations around the mean of -20° (Jagged; 160 trials). After a 2-min interval, participants re-adapted to the same (-20°) visual deviation, which was meant to probe the effect of extended practice in the first Session on the learning capabilities of a second identical memory (A vs A). The results first confirmed that the duration of exposure in the first Session enhanced immediate aftereffects in the Moderate, Long, and Jagged conditions as compared to the Short condition, suggesting that extended practice enhanced retention of the first memory. When comparing the second Session to the first one, results revealed a different pattern of re-adaptation depending on the duration of initial exposure: in the Short condition, there was evidence for facilitated re-adaptation and similar aftereffects. However, in the Moderate, Long and Jagged conditions, re-adaptation was similar and aftereffects were impaired, suggestive of AI. This suggests that extended practice initially enhances memory formation, but comes at the cost of reduced subsequent learning capabilities. One possibility is that AI occurs because extended practice induces the emergence of network-specific homeostatic constraints, which limit subsequent neuroplastic and learning capabilities in the same neural network.

Cerebellar Degeneration Impairs Strategy Discovery but Not Strategy Recall.

The cerebellum is recognized to play a critical role in the automatic and implicit process by which movement errors are used to keep the sensorimotor system precisely calibrated. However, its role in other learning processes frequently engaged during sensorimotor adaptation tasks remains unclear. In the present study, we tested the performance of individuals with cerebellar degeneration on a variant of a visuomotor adaptation task in which learning requires the use of strategic re-aiming, a process that can nullify movement errors in a rapid and volitional manner. Our design allowed us to assess two components of this learning process, the discovery of an appropriate strategy and the recall of a learned strategy. Participants were exposed to a 60° visuomotor rotation twice, with the initial exposure block assessing strategy discovery and the re-exposure block assessing strategy recall. Compared to age-matched controls, individuals with cerebellar degeneration were slower to derive an appropriate aiming strategy in the initial Discovery block but exhibited similar recall of the aiming strategy during the Recall block. This dissociation underscores the multi-faceted contributions of the cerebellum to sensorimotor learning, highlighting one way in which this subcortical structure facilitates volitional action selection.

Visuomotor Adaptation Deficits in Patients with Essential Tremor.

Essential tremor (ET) is a progressive movement disorder whose pathophysiology is not fully understood. Current evidence supports the view that the cerebellum is critically involved in the genesis of the tremor in ET. However, it is still unknown whether cerebellar dysfunction affects not only the control of current movements but also the prediction of future movements through dynamic adaptation toward a changed environment. Here, we tested the capacity of 28 patients with ET to adapt in a visuomotor adaptation task known to depend on intact cerebellar function. We found specific impairments in that task compared to age-matched healthy controls. Adaptation to the visual perturbation was disrupted in ET patients, while de-adaptation, the phase after abrupt removal of the perturbation, developed similarly to control subjects. Baseline tremor-independent motor performance was as well similar to healthy controls, indicating that adaptation deficits in ET patients were not rooted in an inability to perform goal-directed movements. There was no association between clinical severity scores of ET and early visuomotor adaptation abilities. These results provide further evidence that the cerebellum is dysfunctional in ET.

Motor adaptation does not differ when a perturbation is introduced abruptly or gradually.

People continuously adapt their movements to ever-changing circumstances, and particularly in skills training and rehabilitation, it is crucial that we understand how to optimize implicit adaptation in order for these processes to require as little conscious effort as possible. Although it is generally assumed that the way to do this is by introducing perturbations gradually, the literature is ambivalent on the effectiveness of this approach. Here, we tested whether there are differences in motor performance when adapting to an abrupt compared to a ramped visuomotor rotation. Using a within-subjects design, we tested this question under 3 different rotation sizes: 30-degrees, 45-degrees, and 60-degrees, as well as in 3 different populations: younger adults, older adults, and patients with mild cerebellar ataxia. We find no significant differences in either the behavioural outcomes, or model fits, between abrupt and gradual learning across any of the different conditions. Neither age, nor cerebellar ataxia had any significant effect on error-sensitivity either. These findings together indicate that error-sensitivity is not modulated by introducing a perturbation abruptly compared to gradually, and is also unaffected by age or mild cerebellar ataxia.

Direction of visual shift and hand congruency enhance spatial realignment during visuomotor adaptation.

Although prism adaptation has been studied extensively for over 100 years to better understand how the motor system adapts to sensory perturbations, very few studies have systematically studied how the combination of the hand used to adapt, and the direction of visual shift, might influence adaptation. Given that sensory inputs and motor outputs from the same side are processed (at least initially) in the same hemisphere, we wondered whether there might be differences in how people adapt when the hand used and the direction of visual shift were congruent (e.g., adapting to rightward shifting prisms with the right hand), compared to incongruent (e.g., adapting to rightward shifting prisms with the left hand). In Experiment 1 we re-analyzed a previously published dataset (Striemer, Enns, and Whitwell Striemer et al., Cortex 115:201-215, 2019a) in which healthy adults (n = 17) adapted to 17° leftward or rightward optically displacing prisms using their left or right hand (tested in separate sessions, counterbalanced). Our results revealed a "congruency effect" such that adaptation aftereffects were significantly larger for reaches performed without visual feedback (i.e., straight-ahead pointing) when the direction of prism shift and the hand used were congruent, compared to incongruent. We replicated this same congruency effect in Experiment 2 in a new group of participants (n = 25). We suggest that a better understanding of the cognitive and neural mechanisms underlying the congruency effect will allow researchers to build more precise models of visuomotor learning, and may lead to the development of more effective applications of prism adaptation for the treatment of attentional disorders following brain damage.

A Serious Game for the Assessment of Visuomotor Adaptation Capabilities during Locomotion Tasks Employing an Embodied Avatar in Virtual Reality.

The study of visuomotor adaptation (VMA) capabilities has been encompassed in various experimental protocols aimed at investigating human motor control strategies and/or cognitive functions. VMA-oriented frameworks can have clinical applications, primarily in the investigation and assessment of neuromotor impairments caused by conditions such as Parkinson's disease or post-stroke, which affect the lives of tens of thousands of people worldwide. Therefore, they can enhance the understanding of the specific mechanisms of such neuromotor disorders, thus being a potential biomarker for recovery, with the aim of being integrated with conventional rehabilitative programs. Virtual Reality (VR) can be entailed in a framework targeting VMA since it allows the development of visual perturbations in a more customizable and realistic way. Moreover, as has been demonstrated in previous works, a serious game (SG) can further increase engagement thanks to the use of full-body embodied avatars. Most studies implementing VMA frameworks have focused on upper limb tasks and have utilized a cursor as visual feedback for the user. Hence, there is a paucity in the literature about VMA-oriented frameworks targeting locomotion tasks. In this article, the authors present the design, development, and testing of an SG-based framework that addresses VMA in a locomotion activity by controlling a full-body moving avatar in a custom VR environment. This workflow includes a set of metrics to quantitatively assess the participants' performance. Thirteen healthy children were recruited to evaluate the framework. Several quantitative comparisons and analyses were run to validate the different types of introduced visuomotor perturbations and to evaluate the ability of the proposed metrics to describe the difficulty caused by such perturbations. During the experimental sessions, it emerged that the system is safe, easy to use, and practical in a clinical setting. Despite the limited sample size, which represents the main limitation of the study and can be compensated for with future recruitment, the authors claim the potential of this framework as a useful instrument for quantitatively assessing either motor or cognitive impairments. The proposed feature-based approach gives several objective parameters as additional biomarkers that can integrate the conventional clinical scores. Future studies might investigate the relation between the proposed biomarkers and the clinical scores for specific disorders such as Parkinson's disease and cerebral palsy.

Persistence of adaptation following visuomotor training.

Retention tests conducted after sensorimotor adaptation frequently exhibit a rapid return to baseline performance once the altered sensory feedback is removed. This so-called washout of learning stands in contrast with other demonstrations of retention, such as savings on re-learning and anterograde interference effects of initial learning on new learning. In the present study, we tested the hypothesis that washout occurs when there is a detectable discrepancy in retention tests between visual information on the target position and somatosensory information on the position of the limb. Participants were tested following adaptation to gradually rotated visual feedback (15° or 30°). Two different types of targets were used for retention testing, a point target in which a perceptual mismatch is possible, and an arc-target that eliminated the mismatch. It was found that, except when point targets were used, retention test movements were stable throughout aftereffect trials, indicating little loss of information. Substantial washout was only observed in tests with a single point target, following adaptation to a large amplitude 30° rotation. In control studies designed to minimize the use of explicit strategies during learning, we observed similar patterns of decay when participants moved to point targets that suggests that the effects observed here relate primarily to implicit learning. The results suggest that washout in aftereffect trials following visuomotor adaptation is due to a detectable mismatch between vision and somatosensation. When the mismatch is removed experimentally, there is little evidence of loss of information.NEW & NOTEWORTHY Aftereffects following sensorimotor adaptation are important because they bear on the understanding of the mechanisms that subserve forgetting. We present evidence that information loss previously reported during retention testing occurs only when there is a detectable discrepancy between vision and somatosensation and, if this mismatch is removed, the persistence of adaptation is observed. This suggests that washout during aftereffect trials is a consequence of the experimental design rather than a property of the memory system itself.

Inconsistent attentional contexts impair relearning following gradual visuomotor adaptation.

One of the brain's primary functions is to promote actions in dynamic, distracting environments. Because distractions divert attention from our primary goals, we must learn to maintain accurate actions under sensory and cognitive distractions. Visuomotor adaptation is a learning process that restores performance when sensorimotor capacities or environmental conditions are abruptly or gradually altered. Prior work showed that learning to counteract an abrupt perturbation under a particular single- or dual-task setting (i.e., attentional context) was associated with better recall under the same conditions. This suggested that the attentional context was encoded during adaptation and used as a recall cue. The current study investigated whether the attentional context (i.e., single vs. dual task) also affected adaptation and recall to a gradual perturbation, which limited awareness of movement errors. During adaptation, participants moved a cursor to a target while learning to counteract a visuomotor rotation that increased from 0° to 45° by 0.3° each trial, with or without performing a secondary task. Relearning was impaired when the attentional context was different between adaptation and recall (experiment 1), even when the exposure to the attentional context was limited to the early or late half of adaptation (experiment 2). Changing the secondary task did not affect relearning, indicating that the attentional context, rather than specific stimuli or tasks, was associated with better recall performance (experiment 3). These findings highlight the importance of cognitive factors, such as attention, in visuomotor adaptation and have implications for learning and rehabilitation paradigms.NEW & NOTEWORTHY Adaptation acquired under single- or dual-task setting, which created an undivided or divided attentional context, respectively, was impaired when relearning occurred under different conditions (i.e., shifting from a dual to single task). Changes to the attentional context impaired relearning when the initial adaptation was to a gradual perturbation. Explicit awareness of the perturbation was not necessary for this effect to be robust, nor was the effect attributable to changes in the secondary task requirements.

Evidence that endpoint feedback facilitates intermanual transfer of visuomotor force learning by a cognitive strategy.

Humans continuously adapt their movement to a novel environment by recalibrating their sensorimotor system. Recent evidence, however, shows that explicit planning to compensate for external changes, i.e., a cognitive strategy, can also aid performance. If such a strategy is planned in external space, it should improve performance in an effector-independent manner. We tested this hypothesis by examining whether promoting a cognitive strategy during a visual-force adaptation task performed in one hand can facilitate learning for the opposite hand. Participants rapidly adjusted the height of visual bar on screen to a target level by isometrically exerting force on a handle using their right hand. Visuomotor gain increased during the task and participants learned the increased gain. Visual feedback was continuously provided for one group, whereas for another group only the endpoint of the force trajectory was presented. The latter has been reported to promote cognitive strategy use. We found that endpoint feedback produced stronger intermanual transfer of learning and slower response times than continuous feedback. In a separate experiment, we found evidence that aftereffects are reduced when only endpoint feedback is provided, a finding that has been consistently observed when cognitive strategies are used. The results suggest that intermanual transfer can be facilitated by a cognitive strategy. This indicates that the behavioral observation of intermanual transfer can be achieved either by forming an effector-independent motor representation or by sharing an effector-independent cognitive strategy between the hands.NEW & NOTEWORTHY The causes and consequences of cognitive strategy use are poorly understood. We tested whether a visuomotor task learned in a manner that may promote cognitive strategy use causes greater generalization across effectors. Visual feedback was manipulated to promote cognitive strategy use. Learning consistent with cognitive strategy use for one hand transferred to the unlearned hand. Our result suggests that intermanual transfer can result from a common cognitive strategy used to control both hands.

The effects of post-learning alcohol ingestion on human motor memory consolidation.

The neurochemical mechanisms underlying motor memory consolidation remain largely unknown. Based on converging work showing that ethyl alcohol retrogradely enhances declarative memory consolidation, this work tested the hypothesis that post-learning alcohol ingestion would enhance motor memory consolidation. In a within-subject and fully counterbalanced design, participants (n = 24; 12M; 12F) adapted to a gradually introduced visual deviation and ingested, immediately after adaptation, a placebo (PBO), a medium (MED) or high (HIGH) dose of alcohol. The alcohol doses were bodyweight- and gender-controlled to yield peak breath alcohol concentrations of 0.00% in the PBO, ~0.05% in the MED and ~0.095% in the HIGH condition. Retention was evaluated 24 h later through reach aftereffects when participants were sober. The results revealed that retention levels were neither significantly nor meaningfully different in both the MED and HIGH conditions as compared to PBO (all absolute Cohen's dz values < ~0.2; small to negligible effects), indicating that post-learning alcohol ingestion did not alter motor memory consolidation. Given alcohol's known pharmacological GABAergic agonist and NMDA antagonist properties, one possibility is that these neurochemical mechanisms do not decisively contribute to motor memory consolidation. As converging work demonstrated alcohol's retrograde enhancement of declarative memory, the present results suggest that distinct neurochemical mechanisms underlie declarative and motor memory consolidation. Elucidating the neurochemical mechanisms underlying the consolidation of different memory systems may yield insights into the effects of over-the-counter drugs on everyday learning and memory but also inform the development of pharmacological interventions seeking to alter human memory consolidation.

Improved proprioception does not benefit visuomotor adaptation.

Visuomotor adaptation arises when reaching in an altered visual environment, where one's seen hand position does not match their felt (i.e., proprioceptive) hand position in space. Here, we asked if proprioceptive training benefits visuomotor adaptation, and if these benefits arise due to implicit (unconscious) or explicit (conscious strategy) processes. Seventy-two participants were divided equally into 3 groups: proprioceptive training with feedback (PTWF), proprioceptive training no feedback (PTNF), and Control (CTRL). The PTWF and PTNF groups completed passive proprioceptive training, where a participant's hand was moved to an unknown reference location and they judged the felt position of their unseen hand relative to their body midline on every trial. The PTWF group received verbal feedback with respect to their response accuracy on the middle 60% of trials, whereas the PTNF did not receive any feedback during training. The CTRL group did not complete proprioceptive training and instead sat quietly during this time. Following proprioceptive training or time delay, all three groups reached when seeing a cursor that was rotated 30° clockwise relative to their hand motion. The experiment ended with participants completing a series of no-cursor reaches to assess implicit and explicit adaptation. Results indicated that the PTWF group improved the accuracy of their sense of felt hand position following proprioceptive training. However, this improved proprioceptive acuity (i.e., the accuracy of their sense of felt hand) did not benefit visuomotor adaptation, as all three groups showed similar visuomotor adaptation across rotated reach training trials. Visuomotor adaptation arose implicitly, with minimal explicit contribution for all three groups. Together, these results suggest that passive proprioceptive training does not benefit, nor hinder, the extent of implicit visuomotor adaptation established immediately following reach training with a 30° cursor rotation.

The influence of awareness on implicit visuomotor adaptation.

It is well documented that reaches are adapted when reaching with a visuomotor distortion (i.e., rotated cursor feedback). Less clear is the influence of awareness on visuomotor adaptation, where awareness encompasses knowledge of the changes in one's reaches and the visuomotor distortion itself. In the current experiment, we asked if awareness governs the magnitude of implicit (i.e., unconscious) visuomotor adaptation achieved, independent of how the distortion is introduced (i.e., abruptly vs. gradually introduced visuomotor distortion), and hence initial errors experienced. Participants were divided into two groups that differed with respect to how the visuomotor distortion was introduced (i.e., Abrupt vs. Gradual Groups) and reached in a virtual environment where a cursor on the screen misrepresented the position of their hand. Participants completed three blocks of 150 reach training trials in the following order: aligned cursor feedback (baseline), rotated cursor feedback (adaptation) and aligned cursor feedback (washout). For the Abrupt Group, the cursor was immediately rotated 45° clockwise (CW) relative to hand motion in the adaptation block, whereas in the Gradual Group, the 45° cursor rotation was gradually introduced over adaptation trials. Following reach training, participants' awareness of changes in their reaches and the visuomotor distortion were established based on a drawing task, where participants drew the path their hand took to get the cursor on target, as well as a post-experiment questionnaire. Participants were subsequently divided into the following 3 groups: Abrupt-Aware (n = 16), Gradual-Aware (n = 11) and Gradual-Unaware (n = 14). Results revealed that errors differed for the Gradual-Unaware Group at the end of adaptation training compared to the Gradual-Aware Group and at the start of the washout block compared to the Abrupt-Aware Group. Errors in the two aware groups did not differ from each other. These results suggest that awareness may lead to reduced implicit adaptation, regardless of the size of initial errors experienced.

Increased cognitive load in immersive virtual reality during visuomotor adaptation is associated with decreased long-term retention and context transfer.

BACKGROUND: Complex motor tasks in immersive virtual reality using a head-mounted display (HMD-VR) have been shown to increase cognitive load and decrease motor performance compared to conventional computer screens (CS). Separately, visuomotor adaptation in HMD-VR has been shown to recruit more explicit, cognitive strategies, resulting in decreased implicit mechanisms thought to contribute to motor memory formation. However, it is unclear whether visuomotor adaptation in HMD-VR increases cognitive load and whether cognitive load is related to explicit mechanisms and long-term motor memory formation. METHODS: We randomized 36 healthy participants into three equal groups. All groups completed an established visuomotor adaptation task measuring explicit and implicit mechanisms, combined with a dual-task probe measuring cognitive load. Then, all groups returned after 24-h to measure retention of the overall adaptation. One group completed both training and retention tasks in CS (measuring long-term retention in a CS environment), one group completed both training and retention tasks in HMD-VR (measuring long-term retention in an HMD-VR environment), and one group completed the training task in HMD-VR and the retention task in CS (measuring context transfer from an HMD-VR environment). A Generalized Linear Mixed-Effect Model (GLMM) was used to compare cognitive load between CS and HMD-VR during visuomotor adaptation, t-tests were used to compare overall adaptation and explicit and implicit mechanisms between CS and HMD-VR training environments, and ANOVAs were used to compare group differences in long-term retention and context transfer. RESULTS: Cognitive load was found to be greater in HMD-VR than in CS. This increased cognitive load was related to decreased use of explicit, cognitive mechanisms early in adaptation. Moreover, increased cognitive load was also related to decreased long-term motor memory formation. Finally, training in HMD-VR resulted in decreased long-term retention and context transfer. CONCLUSIONS: Our findings show that cognitive load increases in HMD-VR and relates to explicit learning and long-term motor memory formation during motor learning. Future studies should examine what factors cause increased cognitive load in HMD-VR motor learning and whether this impacts HMD-VR training and long-term retention in clinical populations.

Learning the same motor task twice impairs its retention in a time- and dose-dependent manner.

Anterograde interference emerges when two differing tasks are learned in close temporal proximity, an effect repeatedly attributed to a competition between differing task memories. However, recent development alternatively suggests that initial learning may trigger a refractory period that occludes neuroplasticity and impairs subsequent learning, consequently mediating interference independently of memory competition. Accordingly, this study tested the hypothesis that interference can emerge when the same motor task is being learned twice, that is when competition between memories is prevented. In a first experiment, the inter-session interval (ISI) between two identical motor learning sessions was manipulated to be 2 min, 1 h or 24 h. Results revealed that retention of the second session was impaired as compared to the first one when the ISI was 2 min but not when it was 1 h or 24 h, indicating a time-dependent process. Results from a second experiment replicated those of the first one and revealed that adding a third motor learning session with a 2 min ISI further impaired retention, indicating a dose-dependent process. Results from a third experiment revealed that the retention impairments did not take place when a learning session was preceded by simple rehearsal of the motor task without concurrent learning, thus ruling out fatigue and confirming that retention is impaired specifically when preceded by a learning session. Altogether, the present results suggest that competing memories is not the sole mechanism mediating anterograde interference and introduce the possibility that a time- and dose-dependent refractory period-independent of fatigue-also contributes to its emergence. One possibility is that learning transiently perturbs the homeostasis of learning-related neuronal substrates. Introducing additional learning when homeostasis is still perturbed may not only impair performance improvements, but also memory formation.

Different generalization of fast and slow visuomotor adaptation across locomotion and pointing tasks.

Sensorimotor adaptation can involve multiple learning processes with different time courses, and these processes may have different patterns of transfer. In this study, we tested how slow learning and fast learning transfer across tasks, and the specificity of transfer. We tested two natural goal-directed tasks: pointing and walking toward a visible target. We also tested a novel "hand locomotion" task in which subjects used pointing movements to cause simulated self-motion in virtual reality. The hand locomotion task used the same physical movement as pointing, but performed the same function as stepping. During an experimental block, subjects performed alternating training trials with perturbed visual feedback and test trials with no feedback. The test trials were either the same task to measure adaptation, or a different task to measure transfer. Perturbations on adaptation trials varied over time as a sum of sinusoids with different frequencies. Fast learning would be expected to produce equal responses to fast and slow perturbations, while slower learning would dampen responses to higher frequency perturbations. Subjects were generally not aware of the smoothly varying perturbations, but showed detectable adaptation for all three tasks. Only pointing produced significantly different responses to high- and low-frequency perturbations, consistent with slow learning. Adaptation of pointing produced more transfer to the hand locomotion task, which shared the same effector and motor actions, than to the stepping task. The other tasks showed fast learning but little or no slow learning, and equal transfer to tasks with different effector or function. Our results suggest that the slower components of sensorimotor adaptation are more movement specific, while faster learning is more generalizable.