Dataset Information

Motor Cortex Embeds Muscle-like Commands in an Untangled Population Response.

ABSTRACT: Primate motor cortex projects to spinal interneurons and motoneurons, suggesting that motor cortex activity may be dominated by muscle-like commands. Observations during reaching lend support to this view, but evidence remains ambiguous and much debated. To provide a different perspective, we employed a novel behavioral paradigm that facilitates comparison between time-evolving neural and muscle activity. We found that single motor cortex neurons displayed many muscle-like properties, but the structure of population activity was not muscle-like. Unlike muscle activity, neural activity was structured to avoid "tangling": moments where similar activity patterns led to dissimilar future patterns. Avoidance of tangling was present across tasks and species. Network models revealed a potential reason for this consistent feature: low tangling confers noise robustness. Finally, we were able to predict motor cortex activity from muscle activity by leveraging the hypothesis that muscle-like commands are embedded in additional structure that yields low tangling.

SUBMITTER: Russo AA

PROVIDER: S-EPMC5823788 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Motor Cortex Embeds Muscle-like Commands in an Untangled Population Response.

Russo Abigail A AA Bittner Sean R SR Perkins Sean M SM Seely Jeffrey S JS London Brian M BM Lara Antonio H AH Miri Andrew A Marshall Najja J NJ Kohn Adam A Jessell Thomas M TM Abbott Laurence F LF Cunningham John P JP Churchland Mark M MM

Neuron 20180201 4

Primate motor cortex projects to spinal interneurons and motoneurons, suggesting that motor cortex activity may be dominated by muscle-like commands. Observations during reaching lend support to this view, but evidence remains ambiguous and much debated. To provide a different perspective, we employed a novel behavioral paradigm that facilitates comparison between time-evolving neural and muscle activity. We found that single motor cortex neurons displayed many muscle-like properties, but the st ...[more]

PMID: 29398358

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Project description:UNLABELLED:Oscillations in the beta and gamma bands (13-30 Hz; 35-70 Hz) have often been observed in motor cortical outputs that reach the spinal cord, acting on motoneurons and interneurons. However, the frequencies of these oscillations are above the muscle force frequency range. A current view is that the transformation of the motoneuron pool inputs into force is linear. For this reason possible roles for these oscillations are unclear, since if this transformation is linear, the high frequencies in the motoneuron inputs (e.g., 20 Hz from pyramidal tract neurons) would be filtered out by the muscle and have no effect on force control. A biologically inspired mathematical model of the neuromuscular system was used to investigate the impact of high-frequency cortical oscillatory activity on force control. The model simulation results evidenced that a typical motoneuron pool has a nonlinear behavior that enables the decoding of a high-frequency oscillatory input. An input at a single frequency (e.g., beta band) leads to an increase in the steady-state force generated by the muscle. When the input oscillation was amplitude modulated at a given low frequency, the force oscillated at this frequency. In both cases, the mechanism relies on the recruitment and derecruitment of motor units in response to the oscillatory descending drive. Therefore, the results from this study suggest a potential role in force control for cortical oscillations at frequencies at or above the beta band, despite the low-pass behavior of the muscles. SIGNIFICANCE STATEMENT:The role of cortical oscillations in motor control has been a long-standing question, one view being that they are an epiphenomenon. Fast oscillations are known to reach the spinal cord, and hence they have been thought to affect muscle behavior. However, experimental limitations have hampered further advances to explain how they could influence muscle force. An approach for such a challenge was adopted in the present research: to study the problem through computer simulations of an advanced biologically compatible mathematical model. Using such a model, we found that the well-known mechanism of recruitment and derecruitment of the spinal cord motoneurons can allow the muscle to respond to cortical oscillations, suggesting that these oscillations are not epiphenomena in motor control.

Project description:Humans perform various motor tasks by coordinating the redundant motor elements in their bodies. The coordination of motor outputs is produced by motor commands, as well properties of the musculoskeletal system. The aim of this study was to dissociate the coordination of motor commands from motor outputs. First, we conducted simulation experiments where the total elbow torque was generated by a model of a simple human right and left elbow with redundant muscles. The results demonstrated that muscle tension with signal-dependent noise formed a coordinated structure of trial-to-trial variability of muscle tension. Therefore, the removal of signal-dependent noise effects was required to evaluate the coordination of motor commands. We proposed a method to evaluate the coordination of motor commands, which removed signal-dependent noise from the measured variability of muscle tension. We used uncontrolled manifold analysis to calculate a normalized index of synergy. Simulation experiments confirmed that the proposed method could appropriately represent the coordinated structure of the variability of motor commands. We also conducted experiments in which subjects performed the same task as in the simulation experiments. The normalized index of synergy revealed that the subjects coordinated their motor commands to achieve the task. Finally, the normalized index of synergy was applied to a motor learning task to determine the utility of the proposed method. We hypothesized that a large part of the change in the coordination of motor outputs through learning was because of changes in motor commands. In a motor learning task, subjects tracked a target trajectory of the total torque. The change in the coordination of muscle tension through learning was dominated by that of motor commands, which supported the hypothesis. We conclude that the normalized index of synergy can be used to evaluate the coordination of motor commands independently from the properties of the musculoskeletal system.

Dataset Information

Motor Cortex Embeds Muscle-like Commands in an Untangled Population Response.

Publications

Motor Cortex Embeds Muscle-like Commands in an Untangled Population Response.

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