Biology subjects

Krakauer, J. W.

Publications and source records attributed to Krakauer, J. W..

6 recordsLinked to original sources

bioRxiv2018

Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?

Systematic perturbations in motor adaptation tasks are primarily countered by learning from sensory-prediction errors, with secondary contributions from other learning processes. Despite the availability of these additional processes, particularly the use of explicit re-aiming to counteract observed target errors, patients with cerebellar degeneration are surprisingly unable to compensate for their sensory-prediction-error deficits by spontaneously switching to another learning mechanism. We hypothesized that if the nature of the task was changed - by allowing vision of the hand, which eliminates sensory-prediction errors - patients could be induced to preferentially adopt aiming strategies to solve visuomotor rotations. To test this, we first developed a novel visuomotor rotation paradigm that provides participants with vision of their hand in addition to the cursor, effectively setting the sensory-prediction-error signal to zero. We demonstrated in younger healthy controls that this promotes a switch to strategic re-aiming based on target errors. We then showed that with vision of the hand, patients with spinocerebellar ataxia could also switch to an aiming strategy in response to visuomotor rotations, performing similarly to age-matched participants (older controls). Moreover, patients could retrieve their learned aiming solution after vision of the hand was removed, and retain it for at least one year. Both patients and older controls, however, exhibited impaired overall adaptation performance compared to younger healthy controls (age, 18-33), likely due to age-related reductions in spatial and working memory. Moreover, patients failed to generalize, i.e., they were unable to adopt analogous aiming strategies in response to novel rotations, nor could they further improve their performance without vision of the hand. Hence, there appears to be an inescapable obligatory dependence on sensory-prediction-error-based learning - even when this system is impaired in patients with cerebellar degeneration. The persistence of sensory-prediction-error-based learning effectively suppresses a switch to target-error-based learning, which perhaps explains the unexpectedly poor performance by patients with spinocerebellar ataxia in visuomotor adaptation tasks.

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bioRxiv2018

Movement imitation depends on an abstract trajectory representation in dorsal premotor cortex

Humans are particularly good at copying novel and meaningless gestures. The mechanistic and anatomical basis for this specialized imitation ability remains largely unknown. One idea is that imitation occurs by matching body configurations. Here we propose an alternative route to imitation that depends on a body-independent representation of the trajectory path of the end-effector. We studied a group of patients with strokes in the left frontoparietal cortices. We found that they were equally impaired at imitating movement trajectories using the ipsilesional limb (i.e., the non-paretic side) that were cued either by an actor using their whole arm or just by a cursor, suggesting that body configuration is not always critical for imitation and that a representation of abstract trajectory shape may suffice. In addition, imitation ability was uncorrelated to the ability to identify the trajectory shape, suggesting a dissociation between producing trajectory shapes and perceiving their paths. Finally, a lesion-symptom mapping analysis found that imitation deficits were associated with lesions in left dorsal premotor but not parietal cortex. Together, these findings suggest a novel body-independent route to imitation that relies on the ability to plan abstract movement trajectories within dorsal premotor cortex.\n\nSignificance StatementThe ability to imitate is critical for rapidly learning to produce new gestures and actions, but how the brain translates observed movements into motor commands is poorly understood. Examining the ability of patients with strokes affecting the left hemisphere revealed that meaningless gestures can be imitated by succinctly representing only the motion of the hand in space, rather than the posture of the entire arm. Moreover, performance deficits correlated with lesions in dorsal premotor cortex, an area not previously associated with impaired imitation of arm postures. These findings thus describe a novel route to imitation that may also be impaired in some patients with apraxia.

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bioRxiv2017

Practice induces a qualitative change in the memory representation for visuomotor learning

Adaptation of our movements to changes in the environment is known to be supported by multiple learning processes which act in parallel. An implicit process recalibrates motor output to maintain alignment between intended and observed movement outcomes (\"implicit recalibration\"). In parallel, an explicit learning process drives more strategic adjustments of behavior, often by deliberately aiming movements away from an intended target (\"deliberate re-aiming\"). It has long been established that people form a memory for prior experience adapting to a perturbation through the fact that they become able to more rapidly adapt to familiar perturbations (a phenomenon known as \"savings\"). Repeated exposures to the same perturbation can further strengthen savings. It remains unclear, however, which underlying learning process is responsible for this practice-related improvement in savings. We measured the relative contributions of implicit recalibration and deliberate re-aiming to adaptation during multiple exposures to an alternating sequence of perturbations over two days. We found that the implicit recalibration followed an invariant learning curve despite prolonged practice, and thus exhibited no memory of prior experience. Instead, practice led to a qualitative change in re-aiming which, in addition to supporting savings, became able to be expressed rapidly and automatically. This qualitative change appeared to enable participants to form memories for two opposing perturbations, overcoming interference effects that typically prohibit savings when learning multiple, opposing perturbations. Our results are consistent with longstanding theories that frame skill learning as a transition from deliberate to automatic selection of actions.

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bioRxiv2017

Skill Acquisition and Habit Formation as Distinct Effects of Practice

Converging evidence indicates that separate goal-directed and habitual systems compete to control behavior1. However, it has proven difficult to reliably induce habitual behavior in human participants2-4. We reasoned that habits may be present in the form of habitually prepared responses, but are overridden by goal-directed processes, preventing their overt expression. Here we show that latent habits can be unmasked by limiting the time participants have to respond to a stimulus. Participants trained for 4 days on a visuomotor association task. By continuously varying the time allowed to prepare responses, we found that the probability of expressing a learned habit followed a stereotyped time course, peaking 300-600ms after stimulus presentation. This time course was captured by a computational model of response preparation in which habitual responses are automatically prepared at short latency, but are replaced by goal-directed responses at longer latency. A more extensive period of practice (20 days) led to increased habit expression by reducing the average time of movement initiation. These findings refine our understanding of habits, and show that practice can influence habitual behavior in distinct ways: by promoting habit formation, and by modulating the likelihood of habit expression.

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bioRxiv2017

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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bioRxiv2017

Finger recruitment patterns during mirror movements suggest two systems for hand recovery after stroke

Accumulating behavioural and neurophysiological evidence suggests that upper-limb control relies on contributions from both cortical and subcortical motor circuits, with cortical inputs providing fine-finger function and subcortical inputs providing the ability for gross movements, respectively. During recovery of function after stroke, the relative contributions from these pathways may shift. Here we propose that mirror movements that appear after stroke provide a non-invasive assay through which relative contributions from cortical and subcortical pathways towards hand recovery can be studied. We hypothesized that mirror movements, like hand function, are generated by summed contributions from cortical and subcortical pathways, and suggest that subcortical contributions should be characterized by a broad recruitment of fingers, while cortical contributions primarily recruit the homologous finger in the passive hand. In a longitudinal stroke recovery study (Xu et al., 2016), we quantified mirror movements and paretic hand function in 53 stroke patients in the year following unilateral stroke. Mirror movements in the non-paretic hand were exaggerated early after damage (week 2), with paretic finger presses broadly recruiting multiple fingers in the non-paretic hand. On average, however, mirroring in homologous fingers was 1.76 times larger than in non-homologous fingers. Over the year, mirroring in the non-paretic hand progressively normalized with a time-course that mimicked that for the fine-finger deficits in the paretic hand. In comparison, during non-paretic finger presses, the homologous component of mirroring in the paretic hand was reduced early after stroke (week 2) but progressively normalized. Altogether, we conclude that the pattern of mirror movements across homologous and non-homologous fingers reflect the summed contributions of both cortical and subcortical systems, and we discuss the implications of our results towards hand recovery after stroke.

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