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Ivry, R.

Publications and source records attributed to Ivry, R..

11 recordsLinked to original sources

Understanding Strategic Motor Learning as a Process of Hypothesis Testing

Multiple learning processes contribute to successful goal-directed actions under changing physiological states, biomechanical constraints, and environmental contexts. Among these, explicit strategies enable us to discover new movement patterns when existing ones no longer achieve the desired outcome. Yet, how strategies are discovered during motor learning remains unknown. To address this, we developed a novel behavioral paradigm that isolates strategy discovery in response to a range of visuomotor perturbations. This approach revealed that strategy discovery unfolds through an initial period of systematic exploration across multiple candidate strategies, followed by an 'aha' moment in which behavior converges on a stable solution. To account for these dynamics, we developed a computational model based on hypothesis testing in which learners generate and evaluate visuomotor rules to counteract the perturbation. This hypothesis testing model outperformed a range of alternative accounts, including gradual error reduction, win-stay lose-shift learning, and sudden one-shot insight. Together, these findings identify hypothesis testing as a computational mechanism by which humans discover new strategies during motor learning.

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Lesions in the cerebellum impact cross-modal temporal predictions

The cerebellum (CE) supports the encoding of the precise sensory event timing and the generation of temporal predictions. Here we investigated whether focal CE lesions impact temporal predictions in a cross-modal context. Individuals with CE lesion (n=9) and healthy-matched controls (HC) were presented with visuo-auditory stimulus pairs, presented in a temporally regular (predictable) or irregular (unpredictable) manner while EEG was recorded. We hypothesized cross-modal temporal predictions to be mediated by pre-stimulus cerebello-cortical beta-band (12-25Hz) activity. In turn, we expected HC, but not CE patients, to show a modulation of pre-stimulus beta power as a function of temporal prediction. HC showed greater pre-stimulus beta-band suppression in anticipation of sound onsets, and stronger post-stimulus delta- and theta-band (1-4Hz; 4-8Hz) power in the predictable than the unpredictable condition. Furthermore, they displayed a significant modulation of pre-stimulus delta-beta cross-frequency coupling as a function of temporal prediction. These effects were not observed in the CE group. Results confirm that cerebellar lesions impair the generation of temporal predictions in cross-modal (visuo-auditory) stimulus processing, extending the role of cerebellar predictive timing from sensorimotor to motor-independent cross-modal perception.

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Selective recruitment: Evidence for task-dependent gating of inputs to the cerebellum

fMRI studies have documented cerebellar activity across a wide array of tasks. However, the functional contribution of the cerebellum within these task domains remains unclear because cerebellar activity is often studied in isolation. This is problematic, as cerebellar fMRI activity may simply reflect the transmission of neocortical activity through fixed connections. Here we present a new approach that addresses this problem. Rather than focus on task-dependent activity changes in the cerebellum alone, we ask if neocortical inputs to the cerebellum are gated in a task-dependent manner. We hypothesize that input is upregulated when the cerebellum functionally contributes to a task. We first validated this approach using a finger movement task, where the integrity of the cerebellum has been shown to be essential for the coordination of rapid alternating movements but not for force generation. While both neocortical and cerebellar activity increased with increasing speed and force, the speed-related changes in the cerebellum were larger than predicted by an optimized cortico-cerebellar connectivity model. We then applied the same approach in a cognitive domain, assessing how the cerebellum supports working memory. Enhanced gating was associated with the encoding of items in working memory, but not with the manipulation or retrieval of the items. Focusing on task-dependent gating of neocortical inputs to the cerebellum offers a promising approach for using fMRI to understand the specific contributions of the cerebellum to cognitive function.

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Personalized transcranial alternating current stimulation improves sleep quality: Initial Findings

Insufficient sleep is a major health issue. Inadequate sleep is associated with an array of poor health outcomes, including cardiovascular disease, diabetes, obesity, certain forms of cancer, Alzheimers disease, depression, anxiety, and suicidality. Given concerns with typical sedative hypnotic drugs for treating sleep difficulties, there is a compelling need for added alternative interventions. Here, we report results of a non-invasive electrical brain stimulation approach to optimizing sleep involving transcranial alternating current stimulation (tACS). A total of 25 participants (mean age: 46.3, S.D. {+/-}12.4, 15 females) were recruited for a null-stimulation controlled (Control condition), within subjects, randomized crossed design, that included two variants of an active condition involving 15 minutes pre-sleep tACS stimulation. To evaluate the impact on sleep quality, the two active tACS stimulation conditions were designed to modulate sleep-dependent neural activity in the theta/alpha frequency bands, with both stimulation types applied to all subjects in separate sessions. The first tACS condition used a fixed stimulation pattern across all participants, a pattern composed of stimulation at 5Hz and 10Hz. The second tACS condition used a personalized stimulation approach with the stimulation frequencies determined by each individuals peak EEG frequencies in the 4-6Hz and 9-11Hz bands. Personalized tACS stimulation increased sleep quantity (duration) by 22 minutes compared to a Control condition (p=.04), and 19 minutes compared to Fixed tACS stimulation (p=.03). Fixed stimulation did not significantly increase sleep duration compared to Control (mean: 3 minutes; p=0.75). For sleep onset, the Personalized tACS stimulation resulted in reducing the onset by 28% compared to the Fixed tACS stimulation (6 minutes faster, p=.02). For a Poor Sleep sub-group (n=13) categorized with Clinical Insomnia and with a high insomnia severity, Personalized tACS stimulation improved sleep duration by 33 minutes compared to Fixed stimulation (p=0.02), and 30 minutes compared to Control condition (p<0.1). Together, these results suggest that Personalized stimulation improves sleep quantity and time taken to fall asleep relative to Control and Fixed stimulation providing motivation for larger-scale trials for Personalized tACS as a sleep therapeutic, including for those with insomnia.

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The Effect of Perturbation Variability on Sensorimotor Adaptation Does Not Require an Implicit Memory of Errors

In a recent paper1 entitled, "An implicit memory of errors limits human sensorimotor adaptation" Albert and colleagues presented a model in which the adaptive response of the sensorimotor system is flexibly modulated by recent experience, or what they refer to as a "memory of errors". This hypothesis stands in contrast to prevailing models in which automatic and implicit responses to movement errors are relatively insensitive to the statistical properties of the environment2-6. A prime example of this rigidity is that the adaptation system exhibits a saturated response to large errors, resulting in a non-linear motor correction function, a feature that is independent of experience4,5,7. Here we show that the key results reported in Albert et al. are fully explained by presupposing this rigid "motor correction" function without reference to memory-dependent changes in error sensitivity. As such, the evidence presented in Albert et. al. does not support the claim that the history of errors modulates implicit adaptation.

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Differential effects of cerebellar degeneration on feedforward versus feedback control across speech and reaching movements

Errors that result from a mismatch between predicted movement outcomes and sensory afference are used to correct ongoing movements through feedback control and to adapt feedforward control of future movements. The cerebellum has been identified as a critical part of the neural circuit underlying implicit adaptation across a wide variety of movements (reaching, gait, eye movements, and speech). The contribution of this structure to feedback control is less well understood: although it has recently been shown in the speech domain that individuals with cerebellar degeneration produce even larger online corrections for sensory perturbations than control participants, similar behavior has not been observed in other motor domains. Currently, comparisons across domains are limited by different population samples and potential ceiling effects in existing tasks. To assess the relationship between changes in feedforward and feedback control associated with cerebellar degeneration across motor domains, we evaluated adaptive (feedforward) and compensatory (feedback) responses to sensory perturbations in reaching and speech production in human participants of both sexes with cerebellar degeneration and neurobiologically healthy controls. As expected, the cerebellar group demonstrated impaired adaptation in both reaching and speech. In contrast, the groups did not differ in their compensatory response in either domain. Moreover, compensatory and adaptive responses in the cerebellar group were not correlated within or across motor domains. These results point to a general impairment in feedforward control with spared feedback control in cerebellar degeneration. However, the magnitude of feedforward impairments and potential changes in feedback-based control manifest in a domain-specific manner across individuals. Significance StatementThe cerebellum contributes to feedforward updating of movement in response to sensory errors, but its role in feedback control is less understood. Here, we tested individuals with cerebellar degeneration (CD), using sensory perturbations to assess adaptation of feedforward control and feedback gains during reaching and speech production tasks. The results confirmed that CD leads to reduced adaption in both domains. However, feedback gains were unaffected by CD in either domain. Interestingly, measures of feedforward and feedback control were not correlated across individuals within or across motor domains. Together, these results indicate a general impairment in feedforward control with spared feedback control in CD. However, the magnitude of feedforward impairments manifests in a domain-specific manner across individuals.

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Exploring Contextual Interference in Implicit and Explicit Motor Learning

The classic advice given to anyone learning a new skill is \"practice makes perfect.\" While this provides a good general rule to follow, it lacks any detail on what form of practice will efficiently maximize learning. So when faced with the task of acquiring multiple skills, what is the optimal way to learn? Would it be more beneficial to master each skill separately or learn them all at once in an interleaved fashion? A concept known as contextual interference suggests that using a random practice schedule leads to better retention than a blocked one. There are some motor learning studies that are consistent with this hypothesis and some that are not. In order to explore these conflicting results, we applied contextual interference to a simple reaching task that could allow us to observe its effects to various components of motor learning. We had participants learn three different visuomotor rotations and manipulated interference by placing them in groups characterized by how training targets are ordered (blocked vs. random). Using reaction time and hand angle as our measures of performance, we found that participants who experienced a random practice schedule had significant improvements in their ability to retain information, which was manifest as higher levels of implicit adaptation and faster reaction times. However, this did not necessarily mean the information was executed accurately since hand angles did not differ between groups. These findings suggest contextual interference will be most advantageous in situations that require fast explicit recall of a motor plan to use rather than those that emphasize accuracy.

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A Multi-Domain Task Battery Reveals Functional Boundaries in the Human Cerebellum

There is compelling evidence that the human cerebellum is engaged in a wide array of motor and cognitive tasks. A fundamental question centers on whether the cerebellum is organized into distinct functional sub-regions. To address this question, we employed a rich task battery, designed to tap into a broad range of cognitive processes. During four functional magnetic resonance imaging (fMRI) sessions, participants performed a battery of 26 diverse tasks comprising 47 unique conditions. Using the data from this multi-domain task battery, we derived a comprehensive functional parcellation of the cerebellar cortex, and evaluated it by predicting functional boundaries in a novel set of tasks. The new parcellation successfully identified distinct functional sub-regions, providing significant improvements over existing parcellations derived from task-free data. Lobular boundaries, commonly used to summarize functional data, did not coincide with functional subdivisions. This multi-domain task approach offers novel insights into the functional heterogeneity of the cerebellar cortex.

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Intrinsic rewards modulate sensorimotor adaptation

Recent studies have demonstrated that task success signals can modulate behavioral changes during sensorimotor adaptation tasks, primarily through the engagement of explicit processes. In a series of reaching experiments with human participants, we explore a potential interaction between reward-based learning and implicit adaptation, using a method in which feedback is not contingent on task performance. We varied the size of the target to compare conditions in which visual feedback indicated an invariant angular error that either hit or missed the target. Hitting the target attenuated the behavioral changes from adaptation, an effect we attribute to the generation of an intrinsic reward signal. We evaluated two models, one in which reward and adaptation systems operate in parallel, and a second in which reward acts directly on the adaptation system. The results favor the latter, consistent with evidence showing communication, and possible overlap, between neural substrates underlying reward-based learning and sensorimotor adaptation.

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Invariant errors reveal limitations in motor correction rather than constraints on error sensitivity

Implicit sensorimotor adaptation is traditionally described as a process of error reduction, whereby a fraction of the error is corrected for with each movement. Here, in our study of healthy human participants, we characterize two constraints on this learning process: the size of adaptive corrections is only related to error size when errors are smaller than 6{degrees}, and learning functions converge to a similar level of asymptotic learning over a wide range of error sizes. These findings are problematic for current models of sensorimotor adaptation, and point to a new theoretical perspective in which learning is constrained by the size of the error correction, rather than sensitivity to error.

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The Cerebellum Does More Than Sensory-Prediction-Error-Based Learning In Sensorimotor Adaptation Tasks

Individuals with damage to the cerebellum perform poorly in sensorimotor adaptation paradigms. This deficit has been attributed to impairment in sensory-prediction-error-based updating of an internal forward model, a form of implicit learning. These individuals can, however, successfully counter a perturbation when instructed with an explicit aiming strategy. This successful use of an instructed aiming strategy presents a paradox: In adaptation tasks, why dont individuals with cerebellar damage come up with an aiming solution on their own to compensate for their implicit learning deficit? To explore this question, we employed a variant of a visuomotor rotation task in which, prior to executing a movement on each trial, the participants verbally reported their intended aiming location. Compared to healthy controls, participants with spinocerebellar ataxia (SCA) displayed impairments in both implicit learning and aiming. This was observed when the visuomotor rotation was introduced abruptly (Exp. 1) or gradually (Exp. 2). This dual deficit does not appear to be related to the increased movement variance associated with ataxia: Healthy undergraduates showed little change in implicit learning or aiming when their movement feedback was artificially manipulated to produce similar levels of variability (Exp. 3). Taken together the results indicate that a consequence of cerebellar dysfunction is not only impaired sensory-prediction-error-based learning, but also a difficulty in developing and/or maintaining an aiming solution in response to a visuomotor perturbation. We suggest that this dual deficit can be explained by the cerebellum forming part of a network that learns and maintains action-outcome associations across trials.\n\nNew and noteworthyIndividuals with cerebellar pathology are impaired in sensorimotor adaptation. This deficit has been attributed to an impairment in error-based learning, specifically, from a deficit in using sensory prediction errors to update an internal model. Here, we show that these individuals also have difficulty in discovering an aiming solution to overcome their adaptation deficit, suggesting a new role for the cerebellum in sensorimotor adaptation tasks.

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