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Causal Role of Motor Preparation during Error-Driven Learning.

ABSTRACT: Current theories suggest that an error-driven learning process updates trial-by-trial to facilitate motor adaptation. How this process interacts with motor cortical preparatory activity-which current models suggest plays a critical role in movement initiation-remains unknown. Here, we evaluated the role of motor preparation during visuomotor adaptation. We found that preparation time was inversely correlated to variance of errors on current trials and mean error on subsequent trials. We also found causal evidence that intracortical microstimulation during motor preparation was sufficient to disrupt learning. Surprisingly, stimulation did not affect current trials, but instead disrupted the update computation of a learning process, thereby affecting subsequent trials. This is consistent with a Bayesian estimation framework where the motor system reduces its learning rate by virtue of lowering error sensitivity when faced with uncertainty. This interaction between motor preparation and the error-driven learning system may facilitate new probes into mechanisms underlying trial-by-trial adaptation.

SUBMITTER: Vyas S

PROVIDER: S-EPMC7185427 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Causal Role of Motor Preparation during Error-Driven Learning.

Vyas Saurabh S O'Shea Daniel J DJ Ryu Stephen I SI Shenoy Krishna V KV

Neuron 20200212 2

Current theories suggest that an error-driven learning process updates trial-by-trial to facilitate motor adaptation. How this process interacts with motor cortical preparatory activity-which current models suggest plays a critical role in movement initiation-remains unknown. Here, we evaluated the role of motor preparation during visuomotor adaptation. We found that preparation time was inversely correlated to variance of errors on current trials and mean error on subsequent trials. We also fou ...[more]

PMID: 32053768

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Project description:Dystonia is a movement disorder characterized by sustained or intermittent muscle contractions causing abnormal, often repetitive movements, postures, or both. Although dystonia is traditionally associated with basal ganglia dysfunction, recent evidence has been pointing to a role of the cerebellum, a brain area involved in motor control and learning. Cerebellar abnormalities have been correlated with dystonia but their potential causative role remains elusive. Here, we simulated the cerebellar input-output relationship with high-resolution computational modeling. We used a data-driven cerebellar Spiking Neural Network and simulated a cerebellum-driven associative learning task, Eye-Blink Classical Conditioning (EBCC), which is characteristically altered in relation to cerebellar lesions in several pathologies. In control simulations, input stimuli entrained characteristic network dynamics and induced synaptic plasticity along task repetitions, causing a progressive spike suppression in Purkinje cells with consequent facilitation of deep cerebellar nuclei cells. These neuronal processes caused a progressive acquisition of eyelid Conditioned Responses (CRs). Then, we modified structural or functional local neural features in the network reproducing alterations reported in dystonic mice. Either reduced olivocerebellar input or aberrant Purkinje cell burst-firing resulted in abnormal learning curves imitating the dysfunctional EBCC motor responses (in terms of CR amount and timing) of dystonic mice. These behavioral deficits might be due to altered temporal processing of sensorimotor information and uncoordinated control of muscle contractions. Conversely, an imbalance of excitatory and inhibitory synaptic densities on Purkinje cells did not reflect into significant EBCC deficit. The present work suggests that only certain types of alterations, including reduced olivocerebellar input and aberrant PC burst-firing, are compatible with the EBCC changes observed in dystonia, indicating that some cerebellar lesions can have a causative role in the pathogenesis of symptoms.

Dataset Information

Causal Role of Motor Preparation during Error-Driven Learning.

Publications

Causal Role of Motor Preparation during Error-Driven Learning.

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