Biology subjects

Ivry, R. B.

Publications and source records attributed to Ivry, R. B..

At least 37 records · Page 2Linked to original sources

bioRxiv2023

Implicit motor adaptation and perceived hand position without proprioception: A kinesthetic error may be derived from efferent signals

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.

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bioRxiv2022

A Unitary Mechanism Underlies Adaptation to Both Local and Global Environmental Statistics in Time Perception

Our sense of the passage of time 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. 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. TeaserTime perception of humans is shaped by a common mechanism that is sensitive to short-term and long-term environmental changes.

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bioRxiv2022

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{degrees} 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.

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bioRxiv2022

Advanced Feedback Enhances Sensorimotor Adaptation

It is widely recognized that sensorimotor learning is enhanced when the feedback is provided throughout the movement compared to 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.

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bioRxiv2022

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 on a reaching task in which we used a feedback perturbation method that isolates implicit adaptation. The degree of implicit adaptation was quantified as the change in hand angle in the opposite direction of the perturbation, and retention was quantified as the percent of adaptation remaining after visual feedback was extinguished. In two experiments, participants tested under a random practice schedule exhibited slower implicit adaptation, but better retention compared to participants tested under a blocked practice schedule, the signature of contextual interference. 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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bioRxiv2022

Implicit sensorimotor adaptation is preserved in Parkinson's Disease

Our ability to enact successful goal-directed actions involves multiple learning processes. Among these processes, implicit motor adaptation ensures that the sensorimotor system remains finely tuned in response to changes in the body and environment. Whether Parkinsons Disease (PD) impacts implicit motor adaptation remains a contentious area of research: whereas multiple reports show impaired performance in this population, many others show intact performance. While there are a range of methodological differences across studies, one critical issue is that performance in many of the studies may reflect a combination of implicit adaptation and strategic re-aiming. Here, we revisited this controversy using a visuomotor task designed to isolate implicit adaptation. In two experiments, we found that adaptation in response to a wide range of visual perturbations (3{degrees} - 45{degrees}) was similar in PD and matched control participants. Moreover, in a meta-analysis of previously published work, we found that the mean effect size contrasting PD and controls across 16 experiments was not significant. Together, these analyses indicate that implicit adaptation is preserved in PD, offering a fresh perspective on the role of the basal ganglia in sensorimotor learning. Significance statementAmong multiple motor learning processes, implicit adaptation ensures that our motor system remains exquisitely calibrated. Whether Parkinsons disease affects implicit motor adaptation has been a point of controversy. We revisited this issue using a visuomotor task designed to isolate implicit adaptation and found that individuals with PD and matched controls showed indistinguishable performance. A meta-analysis based on data from 16 previous experiments yielded a similar null result, strongly supporting the notion that implicit adaptation is preserved in PD.

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bioRxiv2022

Implicit adaptation is modulated by the relevance of feedback

Given that informative and relevant feedback in the real world is often intertwined with distracting and irrelevant feedback, we asked how the relevancy of visual feedback impacts implicit sensorimotor adaptation. To tackle this question, we presented multiple cursors as visual feedback in a center-out reaching task and varied the task relevance of these cursors. In other words, participants were instructed to hit a target with a specific task-relevant cursor, while ignoring the other cursors. In Experiment 1, we found that reach aftereffects were attenuated by the mere presence of distracting cursors, compared to reach aftereffects in response to a single task-relevant cursor. The degree of attenuation did not depend on the position of the distracting cursors. In Experiment 2, we examined the interaction between task relevance and attention. Participants were asked to adapt to a task-relevant cursor/target pair, while ignoring the task-irrelevant cursor/target pair. Critically, we jittered the location of the relevant and irrelevant target in an uncorrelated manner, allowing us to index attention via how well participants tracked the position of target. We found that participants who were better at tracking the task-relevant target/cursor pair showed greater aftereffects, and interestingly, the same correlation applied to the task-irrelevant target/cursor pair. Together, these results highlight a novel role of task relevancy on modulating implicit adaptation, perhaps by giving greater attention to informative sources of feedback, increasing the saliency of the sensory prediction error.

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bioRxiv2022

Low vision impairs implicit sensorimotor adaptation in response to small errors, but not large errors

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 (i.e., where you see your hand after reaching versus where you expected it to be). Individuals with low vision experience challenges with visuomotor control, but whether they also experience challenges with implicit 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 large visual errors. This result not only underscores an unappreciated motor learning impairment associated with low vision, but also highlights an important constraint on how low-fidelity visual information is processed by the nervous system to enable successful implicit adaptation. New and NoteworthyWhether implicit adaptation is also impacted by visual uncertainty intrinsic to the nervous system remains unknown. To test this, we examined 20 people who live with visual uncertainty in daily life due to low vision on a visuomotor task that isolates implicit adaptation. We found that low vision attenuates adaptation in response to small errors only, paving the way for new developments in rehabilitation and assistive devices for individuals with sensory impairments.

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bioRxiv2021

Proprioceptive Re-alignment drives Implicit Sensorimotor Adaptation

Multiple learning processes contribute to successful goal-directed actions in the face of changing physiological states, biomechanical constraints, and environmental contexts. Amongst these processes, implicit sensorimotor adaptation is of primary importance, ensuring that movements remain well-calibrated and accurate. A large body of work on reaching movements has emphasized how adaptation centers on an iterative process designed to minimize visual errors. The role of proprioception has been largely neglected, thought to play a passive role in which proprioception is affected by the visual error but does not directly contribute to adaptation. Here we present an alternative to this visuo-centric framework, arguing that that implicit adaptation can be understood as minimizing a proprioceptive error, the distance between the perceived hand position and its intended goal. We use this proprioceptive re-alignment model (PReMo) to re-examine many phenomena that have previously been interpreted in terms of learning from visual errors, as well as offer novel accounts for unexplained phenomena. We discuss potential challenges for this new perspective on implicit adaptation and outline a set of predictions for future experimentation.

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bioRxiv2021

kTMP: A New Non-invasive Magnetic Induction Method to Modulate Cortical Excitability.

Non-invasive brain stimulation (NIBS) provides a method for safely perturbing brain activity, and has been employed in basic research to test hypotheses concerning brainbehavior relationships with increasing translational applications. We introduce and evaluate a novel subthreshold NIBS method: kilohertz transcranial magnetic perturbation (kTMP). kTMP is a magnetic induction method that delivers continuous kHz-frequency cortical electric fields (E-fields) which may be amplitude-modulated to potentially mimic electrical activity at endogenous frequencies. We used TMS to compare the amplitude of motor-evoked potentials (MEPs) in a hand muscle before and after kTMP. In Experiment 1, we applied kTMP for 10 min over motor cortex to induce an E-field amplitude of approximately 2.0 V/m, comparing the effects of waveforms at frequencies of 2.0, 3.5, or 5.0 kHz. In Experiments 2 and 3 we used two forms of amplitude-modulated kTMP with a carrier frequency at 3.5 kHz and modulation frequencies of either 20 or 140 Hz. The only percept associated with kTMP was an auditory tone, making kTMP amenable for doubleblind experimentation. Relative to sham stimulation, non-modulated kTMP at 2.0 and 3.5 kHz resulted in an increase in cortical excitability, with Experiments 2 and 3 providing a replication of this effect for the 3.5 kHz condition. Although amplitude-modulated kTMP increased MEP amplitude compared to sham, no enhancement was found compared to non-modulated kTMP. kTMP opens a new experimental NIBS space inducing relatively large amplitude subthreshold E-fields able to increase cortical excitability with minimal sensation.

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bioRxiv2021

Use-dependent biases primarily originate from a contaminated motor plan

Repetition of a specific movement biases subsequent actions towards the recently practiced movement, a phenomenon referred to as use-dependent learning (UDL). UDL has been attributed to shifts in the tuning of neurons in the motor cortex. However, recent studies employing a forced reaction time task, including the eLife article by Marinovic et al (2017), indicate that these biases may also arise from a contaminated motor plan, one that is biased towards the practiced direction. We advanced this line of inquiry, seeking to establish the relative contribution of execution and planning processes to UDL in a center-out reaching task in which participants were able to initiate movements of their own volition. On most trials, the target appeared at a designated "frequent" location; on other trials, the target appeared at one of six "rare" locations. In Experiment 1, participants exhibited a robust movement bias towards the frequent target when movements were self-initiated quickly, but a small movement bias when movements were self-initiated slowly - the signature of a contaminated motor plan. Strikingly, the heading angles were bimodally distributed, with one peak at the frequent target location and the other at the rare target location - a finding reinforced by a re-analysis of two widely cited studies on UDL. Notably, the latter peak was shifted in the frequently practiced direction, a signature of a motor execution bias. To eliminate the contribution of planning-related UDL, we imposed a delay between target onset and movement initiation in Experiment 2. As predicted, the heading angles became unimodally distributed around the rare target. The peak of this distribution was again shifted towards the location of the frequent target, indicative of a persistent bias in motor execution. Taken together, these results highlight two distinct components of UDL even when movements are self-initiated: First, the temporal dynamics underlying movement planning, in which a default plan is progressively overridden by a new plan, produces a pronounced motor planning bias. Second, there is a small, temporally stable bias that may reflect shifts in motor unit tuning.

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bioRxiv2021

Distinct Processing of Sensory Prediction Error and Task Error during Motor Learning

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. Authors summaryWhat information does the brain use to maintain precise calibration of the sensorimotor system? Using a reaching task paired with computational modeling, we find that movements are implicitly recalibrated by errors in predicting both the sensory outcome of movement (i.e., sensory prediction errors) as well as errors in achieving the movement goal (i.e., task errors). Even though task errors alone do not elicit implicit recalibration, they nonetheless modulate implicit recalibration when sensory prediction error is present. The results elucidate an unappreciated interaction between these two sources of error in driving implicit recalibration.

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bioRxiv2021

Left Hemisphere Dominance for Bilateral Kinematic Encoding in the Human Brain

Neurophysiological studies in humans and non-human primates have revealed movement representations in both the contralateral and ipsilateral hemisphere. Inspired by clinical observations, we ask if this bilateral representation differs for the left and right hemispheres. Electrocorticography (ECoG) was recorded in human participants during an instructed-delay reaching task, with movements produced with either the contralateral or ipsilateral arm. Using a cross-validated kinematic encoding model, we found stronger bilateral encoding in the left hemisphere, an effect that was present during preparation and was amplified during execution. Consistent with this asymmetry, we also observed better across-arm generalization in the left hemisphere, indicating similar neural representations for right and left arm movements. Notably, these left hemisphere electrodes were centered over premotor and parietal regions. The more extensive bilateral encoding in the left hemisphere adds a new perspective to the pervasive neuropsychological finding that the left hemisphere plays a dominant role in praxis.

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bioRxiv2021

Moving outside the lab: The viability of conducting sensorimotor learning studies online

Collecting data online via crowdsourcing platforms has proven to be a very efficient way to recruit a large and diverse sample. Studies of motor learning, however, have been largely confined to the lab due to the need for special equipment to record movement kinematics and, as such, are typically only accessible to specific participants (e.g., college students). As a first foray to make motor learning studies accessible to a larger and more diverse audience, we developed an online, web-based platform (OnPoint) to collect kinematic data, serving as a template for researchers to create their own online sensorimotor control and learning experiments. As a proof-of-concept, we asked if fundamental motor learning phenomena discovered in the lab could be replicated online. In a series of three experiments, we observed a close correspondence between the results obtained online with those previously reported from research conducted in the laboratory. This web-based platform paired with online crowdsourcing can serve as a powerful new method for the study of motor control and learning.

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bioRxiv2021

The human cerebellum is essential for modulating perceptual sensitivity based on temporal expectations

A functional benefit of attention is to proactively enhance perceptual sensitivity in space and time. Although attentional orienting has traditionally been associated with cortico-thalamic networks, recent evidence has shown that individuals with cerebellar degeneration (CD) show a reduced reaction time benefit from cues that enable temporal anticipation. While this deficit may reflect impairment in anticipatory motor preparation, it could also arise from cerebellar contribution to attentional modulation in time of perceptual sensitivity. To examine this, we tested CD participants on a non-speeded, challenging perceptual discrimination task, asking if they benefit from temporal cues. Strikingly, the CD group showed no duration-specific perceptual sensitivity benefit when cued by repeated but aperiodic presentation of the target interval. In contrast, they performed similar to controls when cued by a rhythmic stream. This dissociation further specifies the functional domain of the cerebellum and establishes its role in the attentional adjustment of perceptual sensitivity in time.

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bioRxiv2020

Individual differences in proprioception predict the extent of implicit sensorimotor adaptation

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 (biased) sensed hand position realigns with the target. When a visuo-proprioceptive discrepancy is introduced, the sensed hand position is biased towards the visual cursor and the adaptive system nullifies 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). While these results do not favor one hypothesis over the other, they underscore the critical role of proprioception in sensorimotor adaptation, and moreover, motivate a novel perspective on how these proprioceptive constraints drive implicit changes in motor behavior. SIGNIFICANCE STATEMENTWhile the sensorimotor system uses sensory feedback to remain properly calibrated, this learning process is constrained, limited in the maximum degree of plasticity. The factors determining this limit remain elusive. Guided by two hypotheses concerning how visual and proprioceptive information are integrated, 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.

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bioRxiv2020

Hybrid local and distributed coding in PMd/M1 provides separation and interaction of bilateral arm signals

Pronounced activity is observed in both hemispheres of the motor cortex during preparation and execution of unimanual movements. The organizational principles of bi-hemispheric signals and the functions they serve throughout motor planning remain unclear. Using an instructed-delay reaching task in monkeys, we identified two components in population responses spanning PMd and M1. A "dedicated" component, which segregated activity at the level of individual units, emerged in PMd during preparation. It was most prominent following movement when M1 became strongly engaged, and principally involved the contralateral hemisphere. In contrast to recent reports, these dedicated signals solely accounted for divergence of arm-specific neural subspaces. The other "distributed" component mixed signals for each arm within units, and the subspace containing it did not discriminate between arms at any stage. The statistics of the population response suggest two functional layers of the cortical network: one that spans both hemispheres for supporting preparatory and ongoing processes, and another that is predominantly housed in the contralateral hemisphere and specifies unilateral output.

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bioRxiv2020

An associative learning account of sensorimotor adaptation

Traditional associative learning tasks focus on the formation of associations between salient events and arbitrary stimuli that predict those events. This is exemplified in cerebellar-dependent delay eyeblink conditioning, where arbitrary cues such as a light or tone act as conditioning stimuli that predict aversive sensations at the cornea. Here we ask if a similar framework could be applied to another type of cerebellar-dependent sensorimotor learning - sensorimotor adaptation. Models of sensorimotor adaptation posit that the introduction of an environmental perturbation results in an error signal that is used to update an internal model of a sensorimotor map for motor planning. Here we take a step towards an integrative account of these two forms of cerebellar-dependent learning, examining the relevance of core concepts from associative learning for sensorimotor adaptation. Using a visuomotor adaptation reaching task, we paired movement-related feedback with neutral auditory or visual contextual cues that served as conditioning stimuli (CSs). Trial-by trial changes in feedforward movement kinematics exhibited three key signatures of associative learning: Differential conditioning, sensitivity to the CS-US interval, and compound conditioning. Moreover, after compound conditioning, a robust negative correlation was observed between responses to the two elemental CSs of the compound (i.e., overshadowing), consistent with the additivity principle posited by theories of associative learning. The existence of associative learning effects in sensorimotor adaptation provides a proof-of-concept for linking cerebellar- dependent learning paradigms within a common theoretical framework.

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