VTA projections to M1 are essential for reorganization of layer 2-3 network dynamics underlying motor learning

Ghanayim, Amir; Benisty, Hadas; Cohen-Rimon, Avigail; Schwartz, Sivan; Talmon, Ronen; Schiller, Jackie

doi:10.1101/2023.11.22.568212

Cited by 2 publications

References 87 publications

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Effects Of Extrinsic Reward Based Skill Learning On Motor Plasticity

Yadav,

Vassiliadis,

Dubuc

et al. 2024

Preprint

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Human motor skill acquisition is improved by performance feedback and coupling such feedback with extrinsic reward (such as money) can enhance skill learning. However, the neurophysiology underlying such behavioral effect is unclear. To bridge this gap, we assessed the effects of reward on multiple forms of motor plasticity during skill learning. Sixty-five healthy participants divided in three groups performed a pinch-grip skill task with sensory feedback only, sensory and reinforcement feedback or both feedback coupled with an extrinsic monetary reward during skill training. To probe motor plasticity, we applied transcranial magnetic stimulation on the left primary motor cortex at rest before, during and after training in the three groups. We evaluated the amplitude and variability of corticospinal output, GABA-ergic short-intracortical inhibition and use-dependent plasticity before training and at two time points during and after training. At the behavioral level, monetary reward accelerated skill learning. In parallel, corticospinal output became less variable early on during training in the presence of extrinsic reward. Interestingly, this effect was particularly pronounced for participants who were more sensitive to reward, as evaluated in an independent questionnaire. Other measures of motor excitability remained comparable across groups. These findings highlight that a mechanism underlying the benefit of reward on motor skill learning is the fine tuning of early-training resting-state corticospinal variability.SIGNIFICANCE STATEMENTSkill acquisition is enhanced in the presence of reward. Despite its potential clinical relevance for motor rehabilitation, the underlying neurophysiological mechanisms remain largely unexplored. Specifically, whether reward affects the plasticity of motor cortex in the context of skill learning is unclear. We show that reward reduces the variability of corticospinal output at an early stage during training and that this effect correlates with individual sensitivity to reward. Our results suggest that a key mechanism underlying the beneficial effect of reward on motor skill learning may be an increase in the stability of motor output in response to training during early stages of skill learning.

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Effects Of Extrinsic Reward Based Skill Learning On Motor Plasticity

Yadav,

Vassiliadis,

Dubuc

et al. 2024

Preprint

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Learning and Control in Motor Cortex across Cell Types and Scales

Economo,

Komiyama,

Kubota

et al. 2024

J. Neurosci.

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The motor cortex is essential for controlling the flexible movements underlying complex behaviors. Behavioral flexibility involves the ability to integrate and refine new movements, thereby expanding an animal's repertoire. This review discusses recent strides in motor learning mechanisms across spatial and temporal scales, describing how neural networks are remodeled at the level of synapses, cell types, and circuits and across time as animals' learn new skills. It highlights how changes at each scale contribute to the evolving structure and function of neural circuits that accompanies the expansion and refinement of motor skills. We review new findings highlighted by advanced imaging techniques that have opened new vistas in optical physiology and neuroanatomy, revealing the complexity and adaptability of motor cortical circuits, crucial for learning and control. At the structural level, we explore the dynamic regulation of dendritic spines mediating corticocortical and thalamocortical inputs to the motor cortex. We delve into the role of perisynaptic astrocyte processes in maintaining synaptic stability during learning. We also examine the functional diversity among pyramidal neuron subtypes, their dendritic computations and unique contributions to single cell and network function. Further, we highlight how cortical activation is characterized by increased consistency and reduced strength as new movements are learned and how external inputs contribute to these changes. Finally, we consider the motor cortex's necessity as movements unfold over long time scales. These insights will continue to drive new research directions, enhancing our understanding of motor cortical circuit transformations that underpin behavioral changes expressed throughout an animal's life.

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VTA projections to M1 are essential for reorganization of layer 2-3 network dynamics underlying motor learning

Cited by 2 publications

References 87 publications

Effects Of Extrinsic Reward Based Skill Learning On Motor Plasticity

Effects Of Extrinsic Reward Based Skill Learning On Motor Plasticity

Learning and Control in Motor Cortex across Cell Types and Scales

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