RESUMO
Implicit adaptation has been regarded as a rigid process that automatically operates in response to movement errors to keep the sensorimotor system precisely calibrated. This hypothesis has been challenged by recent evidence suggesting flexibility in this learning process. One compelling line of evidence comes from work suggesting that this form of learning is context-dependent, with the rate of learning modulated by error history. Specifically, learning was attenuated in the presence of perturbations exhibiting high variance compared to when the perturbation is fixed. However, these findings are confounded by the fact that the adaptation system corrects for errors of different magnitudes in a non-linear manner, with the adaptive response increasing in a proportional manner to small errors and saturating to large errors. Through simulations, we show that this non-linear motor correction function is sufficient to explain the effect of perturbation variance without referring to an experience-dependent change in error sensitivity. Moreover, by controlling the distribution of errors experienced during training, we provide empirical evidence showing that there is no measurable effect of perturbation variance on implicit adaptation. As such, we argue that the evidence to date remains consistent with the rigidity assumption.
Assuntos
Adaptação Fisiológica , Humanos , Adaptação Fisiológica/fisiologia , Simulação por Computador , Aprendizagem/fisiologia , Desempenho Psicomotor/fisiologia , Biologia Computacional , Movimento/fisiologia , Masculino , Adulto , Modelos NeurológicosRESUMO
Implicit sensorimotor adaptation keeps our movements well calibrated amid changes in the body and environment. We have recently postulated that implicit adaptation is driven by a perceptual error: the difference between the desired and perceived movement outcome. According to this perceptual realignment model, implicit adaptation ceases when the perceived movement outcome-a multimodal percept determined by a prior belief conveying the intended action, the motor command, and feedback from proprioception and vision-is aligned with the desired movement outcome. Here, we examined the role of proprioception in implicit motor adaptation and perceived movement outcome by examining individuals who experience deafferentation (i.e., individuals with impaired proprioception and touch). We used a modified visuomotor rotation task designed to isolate implicit adaptation and probe perceived movement outcomes throughout the experiment. Surprisingly, both implicit adaptation and perceived movement outcome were minimally impacted by chronic deafferentation, posing a challenge to the perceptual realignment model of implicit adaptation.NEW & NOTEWORTHY We tested six individuals with chronic somatosensory deafferentation on a novel task that isolates implicit sensorimotor adaptation and probes perceived movement outcome. Strikingly, both implicit motor adaptation and perceptual movement outcome were not significantly impacted by chronic deafferentation, posing a challenge for theoretical models of adaptation that involve proprioception.
Assuntos
Adaptação Fisiológica , Propriocepção , Desempenho Psicomotor , Humanos , Propriocepção/fisiologia , Adaptação Fisiológica/fisiologia , Masculino , Feminino , Desempenho Psicomotor/fisiologia , Adulto , Pessoa de Meia-Idade , Movimento/fisiologia , Idoso , Distúrbios Somatossensoriais/fisiopatologiaRESUMO
Our duration estimation flexibly adapts to the statistical properties of the temporal context. Humans and non-human species exhibit a perceptual bias towards the mean of durations previously observed as well as serial dependence, a perceptual bias towards the duration of recently processed events. Here we asked whether those two phenomena arise from a unitary mechanism or reflect the operation of two distinct systems that adapt separately to the global and local statistics of the environment. We employed a set of duration reproduction tasks in which the target duration was sampled from distributions with different variances and means. The central tendency and serial dependence biases were jointly modulated by the range and the variance of the prior, and these effects were well-captured by a unitary mechanism model in which temporal expectancies are updated after each trial based on perceptual observations. Alternative models that assume separate mechanisms for global and local contextual effects failed to capture the empirical results.
Assuntos
Percepção do Tempo , Tomada de Decisões , Viés , Estimulação Luminosa/métodos , Percepção VisualRESUMO
Successful goal-directed actions require constant fine-tuning of the motor system. This fine-tuning is thought to rely on an implicit adaptation process that is driven by sensory prediction errors (e.g., where you see your hand after reaching vs. where you expected it to be). Individuals with low vision experience challenges with visuomotor control, but whether low vision disrupts motor adaptation is unknown. To explore this question, we assessed individuals with low vision and matched controls with normal vision on a visuomotor task designed to isolate implicit adaptation. We found that low vision was associated with attenuated implicit adaptation only for small visual errors, but not for large visual errors. This result highlights important constraints underlying how low-fidelity visual information is processed by the sensorimotor system to enable successful implicit adaptation.
Assuntos
Baixa Visão , Humanos , MãosRESUMO
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.
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Aprendizagem , Desempenho Psicomotor , Humanos , Destreza Motora , Adaptação Fisiológica , AclimataçãoRESUMO
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.
Assuntos
Doenças Cerebelares , Doenças Neurodegenerativas , Humanos , Desempenho Psicomotor , Aprendizagem , Cerebelo , Rememoração Mental , Adaptação FisiológicaRESUMO
Implicit motor recalibration allows us to flexibly move in novel and changing environments. Conventionally, implicit recalibration is thought to be driven by errors in predicting the sensory outcome of movement (i.e., sensory prediction errors). However, recent studies have shown that implicit recalibration is also influenced by errors in achieving the movement goal (i.e., task errors). Exactly how sensory prediction errors and task errors interact to drive implicit recalibration and, in particular, whether task errors alone might be sufficient to drive implicit recalibration remain unknown. To test this, we induced task errors in the absence of sensory prediction errors by displacing the target mid-movement. We found that task errors alone failed to induce implicit recalibration. In additional experiments, we simultaneously varied the size of sensory prediction errors and task errors. We found that implicit recalibration driven by sensory prediction errors could be continuously modulated by task errors, revealing an unappreciated dependency between these two sources of error. Moreover, implicit recalibration was attenuated when the target was simply flickered in its original location, even though this manipulation did not affect task error - an effect likely attributed to attention being directed away from the feedback cursor. Taken as a whole, the results were accounted for by a computational model in which sensory prediction errors and task errors, modulated by attention, interact to determine the extent of implicit recalibration.
Assuntos
Movimento , Desempenho Psicomotor , Adaptação Fisiológica , Retroalimentação Sensorial , Motivação , Percepção VisualRESUMO
Binary feedback, providing information solely about task success or failure, can be sufficient to drive motor learning. While binary feedback can induce explicit adjustments in movement strategy, it remains unclear if this type of feedback also induces implicit learning. We examined this question in a center-out reaching task by gradually moving an invisible reward zone away from a visual target to a final rotation of 7.5° or 25° in a between-group design. Participants received binary feedback, indicating if the movement intersected the reward zone. By the end of the training, both groups modified their reach angle by about 95% of the rotation. We quantified implicit learning by measuring performance in a subsequent no-feedback aftereffect phase, in which participants were told to forgo any adopted movement strategies and reach directly to the visual target. The results showed a small, but robust (2-3°) aftereffect in both groups, highlighting that binary feedback elicits implicit learning. Notably, for both groups, reaches to two flanking generalization targets were biased in the same direction as the aftereffect. This pattern is at odds with the hypothesis that implicit learning is a form of use-dependent learning. Rather, the results suggest that binary feedback can be sufficient to recalibrate a sensorimotor map.
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Aprendizagem , Desempenho Psicomotor , Humanos , Generalização Psicológica , Movimento , Recompensa , Retroalimentação Sensorial , Adaptação FisiológicaRESUMO
We introduce a novel perspective on how the cerebellum might contribute to cognition, hypothesizing that this structure supports dynamic transformations of mental representations. In support of this hypothesis, we report a series of neuropsychological experiments comparing the performance of individuals with degenerative cerebellar disorders on tasks that either entail continuous, movement-like mental operations or more discrete mental operations. In the domain of visual cognition, the cerebellar disorders group exhibited an impaired rate of mental rotation, an operation hypothesized to require the continuous manipulation of a visual representation. In contrast, the cerebellar disorders group showed a normal processing rate when scanning items in visual working memory, an operation hypothesized to require the maintenance and retrieval of remembered items. In the domain of mathematical cognition, the cerebellar disorders group was impaired at single-digit addition, an operation hypothesized to primarily require iterative manipulations along a mental number-line; this group was not impaired on arithmetic tasks linked to memory retrieval (e.g. single-digit multiplication). These results, obtained in tasks from two disparate domains, point to a potential constraint on the contribution of the cerebellum to cognitive tasks. Paralleling its role in motor control, the cerebellum may be essential for coordinating dynamic, movement-like transformations in a mental workspace.
Assuntos
Doenças Cerebelares , Doenças Neurodegenerativas , Humanos , Cerebelo , Cognição , Rememoração Mental , Memória de Curto PrazoRESUMO
Repetition of specific movement biases subsequent actions towards the practiced movement, a phenomenon known as use-dependent learning (UDL). Recent experiments that impose strict constraints on planning time have revealed two sources of use-dependent biases, one arising from dynamic changes occurring during motor planning and another reflecting a stable shift in motor execution. Here, we used a distributional analysis to examine the contribution of these biases in reaching. To create the conditions for UDL, the target appeared at a designated 'frequent' location on most trials, and at one of six 'rare' locations on other trials. Strikingly, the heading angles were bimodally distributed, with peaks at both frequent and rare target locations. Despite having no constraints on planning time, participants exhibited a robust bias towards the frequent target when movements were self-initiated quickly, the signature of a planning bias; notably, the peak near the rare target was shifted in the frequently practiced direction, the signature of an execution bias. Furthermore, these execution biases were not only replicated in a delayed-response task but were also insensitive to reward. Taken together, these results extend our understanding of how volitional movements are influenced by recent experience.
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Objetivos , Desempenho Psicomotor , Viés , Humanos , Movimento/fisiologia , Desempenho Psicomotor/fisiologia , RecompensaRESUMO
Recent studies have revealed an upper bound in motor adaptation, beyond which other learning systems may be recruited. The factors determining this upper bound are poorly understood. The multisensory integration hypothesis states that this limit arises from opposing responses to visual and proprioceptive feedback. As individuals adapt to a visual perturbation, they experience an increasing proprioceptive error in the opposite direction, and the upper bound is the point where these two error signals reach an equilibrium. Assuming that visual and proprioceptive feedback are weighted according to their variability, there should be a correlation between proprioceptive variability and the limits of adaptation. Alternatively, the proprioceptive realignment hypothesis states that the upper bound arises when the (visually biased) sensed hand position realigns with the expected sensed position (target). When a visuo-proprioceptive discrepancy is introduced, the sensed hand position is biased toward the visual cursor, and the adaptive system counteracts this discrepancy by driving the hand away from the target. This hypothesis predicts a correlation between the size of the proprioceptive shift and the upper bound of adaptation. We tested these two hypotheses by considering natural variation in proprioception and motor adaptation across individuals. We observed a modest, yet reliable correlation between the upper bound of adaptation with both proprioceptive measures (variability and shift). Although the results do not clearly favor one hypothesis over the other, they underscore the critical role of proprioception in sensorimotor adaptation.NEW & NOTEWORTHY Although the sensorimotor system uses sensory feedback to remain calibrated, this learning process is constrained, limited by the maximum degree of plasticity. The factors determining this limit remain elusive. Guided by two hypotheses, we show that individual differences in the upper bound of adaptation in response to a visual perturbation can be predicted by the bias and variability in proprioception. These results underscore the critical, but often neglected role of proprioception in human motor learning.
Assuntos
Adaptação Fisiológica/fisiologia , Retroalimentação Sensorial/fisiologia , Aprendizagem/fisiologia , Propriocepção/fisiologia , Desempenho Psicomotor/fisiologia , Adolescente , Adulto , Feminino , Humanos , Individualidade , Masculino , Adulto JovemRESUMO
Sensorimotor adaptation is influenced by both the size and variance of error information. In the present study, we varied visual uncertainty and error size in a factorial manner and evaluated their joint effect on adaptation, using a feedback method that avoids inherent limitations with standard visuomotor tasks. Uncertainty attenuated adaptation, but only when the error was small. This striking interaction highlights a novel constraint for models of sensorimotor adaptation. Sensorimotor adaptation is driven by sensory prediction errors, the difference between the predicted and actual feedback. When the position of the feedback is made uncertain, motor adaptation is attenuated. This effect, in the context of optimal sensory integration models, has been attributed to the motor system discounting noisy feedback and thus reducing the learning rate. In its simplest form, optimal integration predicts that uncertainty would result in reduced learning for all error sizes. However, these predictions remain untested since manipulations of error size in standard visuomotor tasks introduce confounds in the degree to which performance is influenced by other learning processes such as strategy use. Here, we used a novel visuomotor task that isolates the contribution of implicit adaptation, independent of error size. In two experiments, we varied feedback uncertainty and error size in a factorial manner. At odds with the basic predictions derived from the optimal integration theory, the results show that uncertainty attenuated learning only when the error size was small but had no effect when the error size was large. We discuss possible mechanisms that may account for this interaction, considering how uncertainty may interact with the relevance assigned to the error signal or how the output of the adaptation system in terms of recalibrating the sensorimotor map may be modified by uncertainty.NEW & NOTEWORTHY Sensorimotor adaptation is influenced by both the size and variance of error information. In the present study, we varied visual uncertainty and error size in a factorial manner and evaluated their joint effect on adaptation, using a feedback method that avoids inherent limitations with standard visuomotor tasks. Uncertainty attenuated adaptation but only when the error was small. This striking interaction highlights a novel constraint for models of sensorimotor adaptation.
Assuntos
Adaptação Fisiológica , Córtex Sensório-Motor/fisiologia , Percepção Visual , Adolescente , Feminino , Humanos , Aprendizagem , Masculino , Desempenho Psicomotor , Incerteza , Adulto JovemRESUMO
Sensorimotor learning is thought to entail multiple learning processes, some volitional and others automatic. A new method to isolate implicit learning involves the use of a "clamped" visual perturbation in which, during a reaching movement, visual feedback is limited to a cursor that follows an invariant trajectory offset from the target by a fixed angle. Despite full awareness that the cursor movement is not contingent on their behavior, as well as explicit instructions to ignore the cursor, systematic changes in motor behavior are observed, and these changes have the signatures of motor adaptation observed in studies using classic visuomotor perturbations. Although it is clear that the response to clamped feedback occurs automatically, it remains unknown whether participants are sensitive to the large deviations in hand position that occur during adaptation. To address this question, we used the clamp method and asked participants to report their hand position after each reach. As expected, we observed robust deviations in hand angle away from the target (average of â¼18°). The hand reports also showed systematic deviations over the course of adaptation, initially attracted toward the visual feedback and then in the opposite direction, paralleling the shift in hand position. However, the shift in perceived hand position was subtle, reaching only â¼2° at asymptote. These results confirm that participants have limited awareness of the behavioral changes that occur during sensorimotor adaptation while revealing the impact of feedforward and feedback signals on their subjective experience.NEW & NOTEWORTHY Sensorimotor adaptation operates in an obligatory manner. Qualitatively, subjective reports obtained after adaptation demonstrate that, in many conditions, participants are unaware of significant changes in behavior. In the present study, we quantified participants' sensitivity to these adaptive changes by obtaining reports of hand position on a trial-by-trial basis. The results confirm that participants are largely unaware of adaptation but also reveal the subtle influence of feedback on their subjective experience.
Assuntos
Adaptação Fisiológica , Mãos/fisiologia , Movimento , Desempenho Psicomotor , Adolescente , Adulto , Feminino , Humanos , Masculino , Percepção VisualRESUMO
Goal-directed movements can fail due to errors in our perceptual and motor systems. While these errors may arise from random noise within these sources, they also reflect systematic motor biases that vary with the location of the target. The origin of these systematic biases remains controversial. Drawing on data from an extensive array of reaching tasks conducted over the past 30 years, we evaluated the merits of various computational models regarding the origin of motor biases. Contrary to previous theories, we show that motor biases do not arise from systematic errors associated with the sensed hand position during motor planning or from the biomechanical constraints imposed during motor execution. Rather, motor biases are primarily caused by a misalignment between eye-centric and the body-centric representations of position. This model can account for motor biases across a wide range of contexts, encompassing movements with the right versus left hand, proximal and distal effectors, visible and occluded starting positions, as well as before and after sensorimotor adaptation.
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It is widely recognized that sensorimotor adaptation is facilitated when feedback is provided throughout the movement compared with when it is provided at the end of the movement. However, the source of this advantage is unclear: continuous feedback is more ecological, dynamic, and available earlier than endpoint feedback. Here, we assess the relative merits of these factors using a method that allows us to manipulate feedback timing independent of actual hand position. By manipulating the onset time of "endpoint" feedback, we found that adaptation was modulated in a non-monotonic manner, with the peak of the function occurring in advance of the hand reaching the target. Moreover, at this optimal time, learning was of similar magnitude as that observed with continuous feedback. By varying movement duration, we demonstrate that this optimal time occurs at a relatively fixed time after movement onset, an interval we hypothesize corresponds to when the comparison of the sensory prediction and feedback generates the strongest error signal.
Assuntos
Retroalimentação Sensorial , Desempenho Psicomotor , Retroalimentação , Adaptação Fisiológica , Aprendizagem , MovimentoRESUMO
Motor adaptation - the process of reducing motor errors through feedback and practice - is an essential feature of human competence, allowing us to move accurately in dynamic and novel environments. Adaptation typically results from sensory feedback, with most learning driven by visual and proprioceptive feedback that arises with the movement. In humans, motor adaptation can also be driven by symbolic feedback. In the present study, we examine how implicit and explicit components of motor adaptation are modulated by symbolic feedback. We conducted three reaching experiments involving over 400 human participants to compare sensory and symbolic feedback using a task in which both types of learning processes could be operative (Experiment 1) or tasks in which learning was expected to be limited to only an explicit process (Experiments 2 and 3). Adaptation with symbolic feedback was dominated by explicit strategy use, with minimal evidence of implicit recalibration. Even when matched in terms of information content, adaptation to rotational and mirror reversal perturbations was slower in response to symbolic feedback compared to sensory feedback. Our results suggest that the abstract and indirect nature of symbolic feedback disrupts strategic reasoning and/or refinement, deepening our understanding of how feedback type influences the mechanisms of sensorimotor learning.
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Deterioration in motor control is a hallmark of aging, significantly contributing to a decline in quality of life. More controversial is the question of whether and how aging impacts sensorimotor learning. We hypothesized that the inconsistent picture observed in the current literature can be attributed to at least two factors. First, aging studies tend to be underpowered. Second, the learning assays used in these experiments tend to reflect, to varying degrees, the operation of multiple learning processes, making it difficult to make inferences across studies. We took a two-pronged approach to address these issues. We first performed a meta-analysis of the sensorimotor adaptation literature focusing on outcome measures that provide estimates of explicit and implicit components of adaptation. We then conducted two well-powered experiments to re-examine the effect of aging on sensorimotor adaptation, using behavioral tasks designed to isolate explicit and implicit processes. Convergently, both approaches revealed a striking dissociation: Older individuals exhibited a marked impairment in their ability to discover an explicit strategy to counteract a visuomotor perturbation. However, they exhibited enhanced implicit recalibration. We hypothesize that the effect of aging on explicit learning reflects an age-related decline in reasoning and problem solving, and the effect of aging on implicit learning reflects age-related changes in multisensory integration. Taken together, these findings deepen our understanding of the impact of aging on sensorimotor learning.
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Sensorimotor adaptation is essential for keeping our movements well calibrated in response to changes in the body and environment. For over a century, researchers have studied sensorimotor adaptation in laboratory settings that typically involve small sample sizes. While this approach has proved useful for characterizing different learning processes, laboratory studies are not well suited for exploring the myriad of factors that may modulate human performance. Here, using a citizen science website, we collected over 2,000 sessions of data on a visuomotor rotation task. This unique dataset has allowed us to replicate, reconcile and challenge classic findings in the learning and memory literature, as well as discover unappreciated demographic constraints associated with implicit and explicit processes that support sensorimotor adaptation. More generally, this study exemplifies how a large-scale exploratory approach can complement traditional hypothesis-driven laboratory research in advancing sensorimotor neuroscience.
Assuntos
Ciência do Cidadão , Desempenho Psicomotor , Humanos , Desempenho Psicomotor/fisiologia , Aprendizagem/fisiologia , Movimento/fisiologia , RotaçãoRESUMO
Implicit sensorimotor adaptation keeps our movements well-calibrated amid changes in the body and environment. We have recently postulated that implicit adaptation is driven by a perceptual error: the difference between the desired and perceived movement outcome. According to this perceptual re-alignment model, implicit adaptation ceases when the perceived movement outcome - a multimodal percept determined by a prior belief conveying the intended action, the motor command, and feedback from proprioception and vision - is aligned with the desired movement outcome. Here, we examined the role of proprioception in implicit motor adaptation and perceived movement outcome by examining individuals who lack proprioception. We used a modified visuomotor rotation task designed to isolate implicit adaptation and probe perceived outcome throughout the experiment. Surprisingly, implicit adaptation and perceived outcome were minimally impacted by deafferentation, posing a challenge to the perceptual re-alignment model of implicit adaptation.