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Leow, L.-A.

Publications and source records attributed to Leow, L.-A..

16 recordsLinked to original sources

Musical training improves planning and robustness of sequence learning

Musicians demonstrate advantages in acquiring motor sequences, showing faster learning and better explicit sequence knowledge than non-musicians. However, it is unclear whether this advantage extends beyond acquisition to the consolidation phase, which is when newly learned skills stabilize and become resistant to interference. Additionally, while interference from executing competing motor tasks is well-established, less is known about whether purely sensory information presented after learning can disrupt consolidation of a bimodal motor sequence. We investigated how post-acquisition sensory interference affects performance of a learned audio-visual sequence, and whether musical training moderates this vulnerability. Participants first learned an explicit sequence in a serial reaction time task using synchronous, informative audio-visual cues. After a brief consolidation period, they were randomly assigned to one of four observational conditions that manipulated the relationship between auditory and visual streams. Motor performance was then reassessed. Post-acquisition sensory interference impaired subsequent motor performance, but this effect was modality-specific: it was driven primarily by manipulations to the task-relevant visual stream, while auditory interference alone had no credible effect. Distributional analysis revealed that learning involved a strategic shift from reactive to anticipatory responding. Critically, participants with musical training showed an earlier and consistently higher reliance on anticipatory responses than those without, demonstrating a more rapid adoption of predictive motor control. These findings demonstrate that newly formed sensorimotor memories are selectively vulnerable to interference in task-relevant modalities. Furthermore, our work provides a candidate mechanistic account for the musician advantage in sequence learning, linking it to faster development of predictive motor strategies during consolidation.

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Dopamine alters motor learning performance in the presence and absence of feedback

We often choose to learn motor skills not only because of some external reward, but also because motor learning, in and of itself, is satisfying. While dopamine is thought to drive reward-based motor learning, it remains unclear whether dopamine is implicated in motor learning under conditions ostensibly driven by intrinsic rewards/motivation (i.e., in the absence of extrinsic feedback or reward). Here, by pharmacologically manipulating dopamine using the dopamine precursor Levodopa, we investigated the role of dopamine in an explicit motor learning task guided by internally determined signals of performance success, by removing intrinsic feedback about task success. Specifically, we asked participants to strategically aim away from presented targets by various instructed angles: a form of explicit motor learning that contributes to performance in the classic visuomotor rotation task. In the feedback condition, targets jumped mid-movement by the instructed angle, such that success in target hitting depended on successfully aiming away by the instructed angle. In the no-feedback condition, intrinsic feedback about task success was removed by having targets disappear mid-movement, such that participants could not know if they succeeded at hitting the targets or not. We found that dopamine altered performance, both with and without task feedback about task success. This provides direct evidence for a role of dopamine in motor learning driven by internal task goals.

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Time affects a time-consuming, flexible component and a fast, inflexible component of sensorimotor adaptation.

Prior learning can impair future learning when the requirements of the two memories conflict, a phenomenon termed anterograde interference. In sensorimotor adaptation, the passage of time between initial and future learning can reduce such interference effects. However, we still do not fully understand how time affects learning, as some studies found no effects of time on interference. One possible explanation for such inconclusive findings is that time affects distinct processes underpinning sensorimotor adaptation differently, and these processes may compensate for each others effects on behaviour. Here, we used task manipulations that (1) dissociate adaptation processes driven by task errors from adaptation processes driven by sensory prediction errors, and (2) separate the task-error driven adaptation processes into a flexible component that could not be acquired under time-pressure, or a less-flexible component that could not be acquired under time-pressure. The time between initial and subsequent learning seemed to alter both the flexible and inflexible components of adaptation driven by task errors. Time also led to a small reduction of interference arising from sensory prediction errors. Thus, we provide evidence that multiple components of sensorimotor adaptation are sensitive to the passage of time.

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Sounds and Sights in Sequence Learning: Can Accessory Auditory Cues Enhance Motor Task Performance?

Motor sequence learning, or the ability to learn and remember sequences of actions, such as the sequence of actions required to tie ones shoelaces, is ubiquitous to everyday life. Contemporary research on motor sequence learning has been largely unimodal, ignoring the possibility that our nervous system might benefit from sensory inputs from multiple modalities. In this study, we investigated the properties of motor sequence learning in response to auditory-visual stimuli. We found that sequence learning with auditory-visual stimuli showed a hallmark feature of traditional unimodal sequence learning tasks: sensitivity to stimulus timing, where lengthier interstimulus intervals of 500 ms improved sequence learning compared to briefer interstimulus intervals of 200 ms. Consistent with previous findings, we also found that auditory-visual stimuli improved learning compared to a unimodal visual-only condition. Furthermore, the informativeness of the auditory stimuli was important, as auditory stimuli which predicted the location of visual cues improved sequence learning compared to uninformative auditory stimuli which did not predict the location of the visual cues. Our findings suggest a potential utility of leveraging audio-visual stimuli in sequence learning interventions to enhance skill acquisition in education and rehabilitation contexts.

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Enhanced neural representation of reach target direction for high reward magnitude but not high target probability.

Many characteristics of goal-directed movements, such as their initiation time, initial direction, and speed, are influenced both by the details of previously executed movements (i.e. action history), and by the degree to which previous movements were rewarded or punished (i.e. reward history). In reinforcement learning terms, when movements are externally cued, action and reward history jointly define the probability and magnitude of positive/negative outcomes of available options, and therefore their pre-stimulus expected value. To dissociate which of these neurocomputational variables influence sensorimotor brain processing, we studied how reach behaviour and evoked brain responses are affected by independent manipulations of action and reward history. We found that movements were initiated earlier both for more frequently repeated targets and targets associated with higher reward magnitude, but only movements to highly rewarded targets had higher movement speeds. Classical visually-evoked encephalographic (EEG) potentials (P1/N1) were not affected by either reward magnitude or target probability. There were, however, amplified midline ERP responses at centroparietal electrodes for rewarded targets and movements compared to control, but no differences between more frequently presented targets and control. Critically, the spatial precision of decoded target locations extracted from a multivariate linear decoding model of EEG data was greater for target locations associated with higher reward magnitude than for control target locations ([~]150-300ms after target presentation). Again, there were no differences in the precision of decoded target direction representations between more frequent target locations and control target locations. These data suggest that the expected reward magnitude associated with an action, rather than its long-run expected value, determines the precision of early sensorimotor processing. Significance StatementWe move more quickly and more accurately toward goals that we value more highly, and this is due partly to enhanced motor preparation. However, our expectations about the value of an action depend both on the probability of its requirement and the magnitude of the reward associated with it. Here we disentangled the influence of reward magnitude and probability on early sensorimotor processing via a multivariate linear decoding approach to extract target direction from scalp encephalograms. We found that the spatial precision of decoded target direction was greater for high reward targets but not for more probable targets. Thus, early sensorimotor processing is sharpened when the magnitude of reward associated with movement to a cued target is high. HighlightsO_LIThe direction of movement can be reliably decoded from the scalp EEG from [~]80ms after target presentation. C_LIO_LIThe neural representation of movement direction is more precise for targets that are associated with high reward, but not for targets that are more probable. C_LIO_LIThe magnitude of reward associated with movement to a presented target, rather than the long-run expected value of the movement, sharpens the spatial precision of early sensorimotor processing. C_LI

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Intensity-dependent effects of tDCS on motor learning are related to dopamine

Non-invasive brain stimulation techniques, such as transcranial direct current stimulation (tDCS), are popular methods for inducing neuroplastic changes to alter cognition and behaviour. One challenge for the field is to optimise stimulation protocols to maximise benefits. For this to happen, we need a better understanding of how stimulation modulates cortical functioning/behaviour. To date, there is increasing evidence for a dose-response relationship between tDCS and brain excitability, however how this relates to behaviour is not well understood. Even less is known about the neurochemical mechanisms which may drive the dose-response relationship between stimulation intensities and behaviour. Here, we examine the effect of three different tDCS stimulation intensities (1mA, 2mA, 4mA anodal motor cortex tDCS) administered during the explicit learning of motor sequences. Further, to assess the role of dopamine in the dose-response relationship between tDCS intensities and behaviour, we examined how pharmacologically increasing dopamine availability, via 100mg of levodopa, modulated the effect of stimulation on learning. In the absence of levodopa, we found that 4mA tDCS improved and 1mA tDCS impaired acquisition of motor sequences relative to sham stimulation. Conversely, levodopa reversed the beneficial effect of 4mA tDCS. This effect of levodopa was no longer evident at the 48-hour follow-up, consistent with previous work characterising the persistence of neuroplastic changes in the motor cortex resulting from combining levodopa with tDCS. These results provide the first direct evidence for a role of dopamine in the intensity-dependent effects of tDCS on behaviour.

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Dopamine alters the effect of brain stimulation on decision-making

Non-invasive brain stimulation techniques, such as transcranial direct current stimulation (tDCS), show promise in treating cognitive and behavioural impairments in clinical conditions. However, optimisation of such clinical applications requires a better understanding of how tDCS alters cognition and behaviour. Existing evidence implicates dopamine in the way tDCS alters brain activity and plasticity, however, there is as yet no causal evidence for a role of dopamine in tDCS effects on cognition and behaviour. Here, in a preregistered, double-blinded study, we examined how pharmacologically manipulating dopamine altered the effect of tDCS on the speed-accuracy trade-off, which taps ubiquitous strategic cognitive processes. Cathodal tDCS was delivered over the left prefrontal cortex and the superior medial frontal cortex before participants completed a dot-motion task, deciding the direction of moving dots under instructions to emphasize speed, accuracy, or both. We leveraged computational modelling to uncover how our manipulations altered latent decisional processes driving the speed-accuracy tradeoff. We show that dopamine in combination with tDCS (but not tDCS alone, nor dopamine alone) not only impaired decision accuracy, but also impaired discriminability, which suggests that these manipulations altered the encoding or representation of discriminative evidence. This is, to the best of our knowledge, the first direct evidence implicating dopamine in the way tDCS affects cognition and behaviour. Significance statementTranscranial direct current stimulation (tDCS) can improve cognitive and behavioural impairments in clinical conditions, however better understanding of its mechanisms is required to optimise future clinical applications. Here, using a pharmacological approach to manipulate brain dopamine levels in healthy adults, we demonstrate a role for dopamine in the effects of tDCS in the speed-accuracy trade-off, a strategic cognitive process ubiquitous in many contexts. In doing so, we provide direct evidence implicating dopamine in the way tDCS affects cognition and behaviour.

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Dopamine increases accuracy and lengthens deliberation time in explicit motor skill learning.

Although animal research implicates a central role for dopamine in motor skill learning, a direct causal link has yet to be established in neurotypical humans. Here, we tested if a pharmacological manipulation of dopamine alters motor learning, using a paradigm which engaged explicit, goal-directed strategies. Participants (27 females, 11 males, aged 18-29 years) first consumed either 100mg of Levodopa (n=19), a dopamine precursor that increases dopamine availability, or placebo (n=19). Then, during training, participants learnt the explicit strategy of aiming away from presented targets by instructed angles of varying sizes. Targets shifted mid-movement by the instructed aiming angle. Task success was thus contingent upon aiming accuracy. The effect of the dopamine manipulations on skill learning was assessed during training, and at an overnight follow-up. Increasing dopamine availability improved aiming accuracy and lengthened reaction times, particularly for larger, more difficult aiming angles, both at training, and at follow-up. Results support the proposal that dopamine is important in decisions to engage instrumental motivation to optimise performance, particularly when learning to execute goal-directed strategies in motor skill learning.

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Supplementary motor area contributions to rhythm perception

Timing is everything, but our understanding of the neural mechanisms of timing remains limited, particularly for timing of sequences. Temporal sequences can be represented relative to a recurrent beat (beat-based or relative timing), or as a series of absolute durations (non-beat-based or absolute timing). Neuroimaging work suggests involvement of the basal ganglia, supplementary motor area (SMA), the premotor cortices, and the cerebellum in both beat- and non-beat-based timing. Here we examined how beat-based timing and non-beat-based sequence timing were affected by modulating excitability of the supplementary motor area, the right cerebellum, and the bilateral dorsal premotor cortices, using transcranial direct current stimulation (tDCS). Participants were subjected to a sham stimulation session, followed an active stimulation session where anodal or cathodal 2mA tDCS was applied to the SMA, right premotor cortex, left premotor cortex, or the cerebellum. During both sessions, participants discriminated changes in rhythms which differentially engage beat-based or non-beat-based timing. Rhythm discrimination performance was improved by increasing SMA excitability, and impaired by decreasing SMA excitability. This polarity-dependent effect on rhythm discrimination was absent for cerebellar or premotor cortex stimulation, suggesting a crucial role of the SMA and/or its functionally connected networks in rhythmic timing mechanisms.

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Acoustic stimulation increases implicit adaptation in sensorimotor adaptation

Sensorimotor adaptation is an important part of our ability to perform novel motor tasks (i.e., learning of motor skills). Efforts to improve adaptation in healthy and clinical patients using non-invasive brain stimulation methods have been hindered by interindividual and intra-individual variability in brain susceptibility to stimulation. Here, we explore unpredictable loud acoustic stimulation as an alternative method of modulating brain excitability to improve sensorimotor adaptation. In two experiments, participants moved a cursor towards targets, and adapted to a 30{degrees} rotation of cursor feedback, either with or without unpredictable acoustic stimulation. Acoustic stimulation improved initial adaptation to sensory prediction errors in Study 1, and improved overnight retention of adaptation in Study 2. Unpredictable loud acoustic stimulation might thus be a potent method of modulating sensorimotor adaptation in healthy adults.

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Task errors drive memories that improve sensorimotor adaptation.

Traditional views on how humans adapt movements to perturbations of sensory feedback emphasize a fundamental role for automatic, implicit correction of sensory prediction errors. However, it is now clear that adaptive behaviour also involves deliberate, strategic movement corrections. Such strategic processes have recently been argued to underlie the latent retention of sensorimotor adaptation, evident in improved adaptation to previously encountered perturbations; a phenomenon termed "savings". It remains unclear, however, whether savings results from prior experience of sensory prediction errors, task errors, or both. Here, we used perturbations of target locations and hand position feedback during reaching to dissociate the contributions of task and sensory prediction errors to latent sensorimotor memory. We show that prior learning to correct for task errors is required to improve adaptation to rotated hand position feedback, whereas a history of sensory prediction errors is neither sufficient nor obligatory for savings. A history of correcting for task errors, induced by experimentally perturbing the target location instead of perturbing sensory feedback of movement, improved adaptation to visuomotor perturbations that were never before encountered. Limiting movement preparation time further showed that this learning consists of two distinct components: 1) a strategic component that is flexible enough to facilitate corrective responses in the opposite direction, but that requires substantial preparation time, and 2) a set of inflexible, cached, stimulus-response associations between targets and reach directions, that can be expressed under time-pressure when similar task conditions are experienced. The results emphasise that adaptive responses to sensorimotor perturbations take multiple forms.

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Triggering mechanisms for motor actions: A mini meta-analysis and experimental data.

Motor actions can be released much sooner than normal when the go-signal is of very high intensity (> 100dBa). Although statistical evidence from individual studies has been mixed, it has been assumed that sternocleidomastoid (SCM) muscle activity could be used to distinguish between two neural circuits involved in movement triggering. We summarized meta-analytically the available evidence for this hypothesis, comparing the difference in premotor reaction time (RT) of actions where SCM activity was elicited (SCM+ trials) by loud acoustic stimuli against trials in which it was absent (SCM- trials). We found ten studies, all reporting comparisons between SCM+ and SCM- trials. Our mini meta-analysis showed that premotor RTs are faster in SCM+ than in SCM- trials. We also present experimental data showing the effects of foreperiod predictability can induce differences in RT that would be of similar size to those attributed to the activation of different neurophysiological pathways to trigger prepared actions. We discuss plausible physiological mechanisms that would explain differences in premotor RTs between SCM+ and SCM-trials.

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Task errors contribute to implicit remapping in sensorimotor adaptation

Perturbations of sensory feedback evoke sensory prediction errors (discrepancies between predicted and actual sensory outcomes of movements), and reward prediction errors (discrepancies between predicted rewards and actual rewards). Sensory prediction errors result in obligatory remapping of the relationship between motor commands and predicted sensory outcomes. The role of reward prediction errors in sensorimotor adaptation is less clear. When moving towards a target, we expect to obtain the reward of hitting the target, and so we experience a reward prediction error if the perturbation causes us to miss it. These discrepancies between desired task outcomes and actual task outcomes, or \"task errors\", are thought to drive the use of strategic processes to restore success, although their role is not fully understood. Here, we investigated the role of task errors in sensorimotor adaptation: during target-reaching, we either removed task errors by moving the target mid-movement to align with cursor feedback of hand position, or enforced task error by moving the target away from the cursor feedback of hand position. Removing task errors not only reduced the rate and extent of adaptation during exposure to the perturbation, but also reduced the amount of post-adaptation implicit remapping. Hence, task errors contribute to implicit remapping resulting from sensory prediction errors. This suggests that the system which implicitly acquires new sensorimotor maps via exposure to sensory prediction errors is also sensitive to reward prediction errors.

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The primary motor cortex is critical for the retention of implicit sensorimotor adaptation

Sensorimotor adaptation, or adaptation of movements to external perturbations, is thought to involve the primary motor cortex (M1). In addition to implicit error-driven remapping, explicit re-aiming strategies also contribute to sensorimotor adaptation. However, no studies to date have examined the role of M1 in implicit learning in isolation from explicit strategies. Because the application of explicit strategies requires time, it is possible to emphasise implicit learning by controlling the time available to prepare movement. Here, we examined the role of M1s role in implicit adaptation to rotated visual feedback whilst suppressing the use of explicit re-aiming strategies by limiting movement preparation times to less than 350ms. Perturbing M1 activity via single-pulse TMS during adaptation to a 30 {degrees} rotation of visual feedback did not alter the rate or extent of error compensation, but elicited poorer retention in post-adaptation trials with no perturbation. This work shows that M1 is critical in the retention of new visuomotor maps as a result of implicit adaptation to a perturbation in sensory feedback when strategic error correction processes are suppressed.\n\nHighlightsO_LIAdaptation of movements to perturbations occurs through explicit and implicit processes.\nC_LIO_LIHere, explicit strategies were suppressed by shortening movement preparation time.\nC_LIO_LIPerturbing motor cortex (M1) with TMS selectively impaired retention but not acquisition of sensorimotor adaptation.\nC_LIO_LIM1 plays a crucial role in retention of sensorimotor adaptation obtained via implicit learning.\nC_LI

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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{degrees} 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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Estimating the implicit component of visuomotor rotation learning by constraining movement preparation time.

When sensory feedback is perturbed, accurate movement is restored by a combination of implicit processes and deliberate re-aiming to strategically compensate for errors. Here, we directly compare two methods used previously to dissociate implicit from explicit learning on a trial-by-trial basis: 1) asking participants to report the direction that they aim their movements, and contrasting this with the directions of the target and the movement that they actually produce, 2) manipulating movement preparation time. By instructing participants to re-aim without a sensory perturbation, we show that re-aiming is possible even with the shortest possible preparation times, particularly when targets are narrowly distributed. Nonetheless, re-aiming is effortful and comes at the cost of increased variability, so we tested whether constraining preparation time is sufficient to suppress strategic re-aiming during adaptation to visuomotor rotation with a broad target distribution. The rate and extent of error reduction under preparation time constraints were similar to estimates of implicit learning obtained from self-report without time pressure, suggesting that participants chose not to apply a re-aiming strategy to correct visual errors under time pressure. Surprisingly, participants who reported aiming directions showed less implicit learning according to an alternative measure, obtained during trials performed without visual feedback. This suggests that the process of reporting can affect the extent or persistence of implicit learning. The data extend existing evidence that restricting preparation time can suppress explicit re-aiming, and provide an estimate of implicit visuomotor rotation learning that does not require participants to report their aiming directions.\n\nNew and NoteworthyDuring sensorimotor adaptation, implicit, error-driven learning can be isolated from explicit strategy-driven re-aiming by subtracting self-reported aiming directions from movement directions, or by restricting movement preparation time. Here, we compared the two methods. Restricting preparation times did not eliminate re-aiming, but was sufficient to suppress reaiming during adaptation with widely-distributed targets. The self-report method produced a discrepancy in implicit learning estimated by subtracting aiming directions, and implicit learning measured in no-feedback trials.

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