Dataset Information

Presynaptic gating of monkey proprioceptive signals for proper motor action.

ABSTRACT: Our rich behavioural repertoire is supported by complicated synaptic connectivity in the central nervous system, which must be modulated to prevent behavioural control from being overwhelmed. For this modulation, presynaptic inhibition is an efficient mechanism because it can gate specific synaptic input without interfering with main circuit operations. Previously, we reported the task-dependent presynaptic inhibition of the cutaneous afferent input to the spinal cord in behaving monkeys. Here, we report presynaptic inhibition of the proprioceptive afferent input. We found that the input from shortened muscles is transiently facilitated, whereas that from lengthened muscles is persistently reduced. This presynaptic inhibition could be generated by cortical signals because it started before movement onset, and its size was correlated with the performance of stable motor output. Our findings demonstrate that presynaptic inhibition acts as a dynamic filter of proprioceptive signals, enabling the integration of task-relevant signals into spinal circuits.

SUBMITTER: Tomatsu S

PROVIDER: S-EPMC10600222 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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Presynaptic gating of monkey proprioceptive signals for proper motor action.

Tomatsu Saeka S Kim GeeHee G Kubota Shinji S Seki Kazuhiko K

Nature communications 20231025 1

Our rich behavioural repertoire is supported by complicated synaptic connectivity in the central nervous system, which must be modulated to prevent behavioural control from being overwhelmed. For this modulation, presynaptic inhibition is an efficient mechanism because it can gate specific synaptic input without interfering with main circuit operations. Previously, we reported the task-dependent presynaptic inhibition of the cutaneous afferent input to the spinal cord in behaving monkeys. Here, ...[more]

PMID: 37880215

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Project description:Diverse locomotor behaviors emerge from the interactions between the spinal central pattern generator (CPG), descending brain signals and sensory feedback. Salamander motor behaviors include swimming, struggling, forward underwater stepping, and forward and backward terrestrial stepping. Electromyographic and kinematic recordings of the trunk show that each of these five behaviors is characterized by specific patterns of muscle activation and body curvature. Electrophysiological recordings in isolated spinal cords show even more diverse patterns of activity. Using numerical modeling and robotics, we explored the mechanisms through which descending brain signals and proprioceptive feedback could take advantage of the flexibility of the spinal CPG to generate different motor patterns. Adapting a previous CPG model based on abstract oscillators, we propose a model that reproduces the features of spinal cord recordings: the diversity of motor patterns, the correlation between phase lags and cycle frequencies, and the spontaneous switches between slow and fast rhythms. The five salamander behaviors were reproduced by connecting the CPG model to a mechanical simulation of the salamander with virtual muscles and local proprioceptive feedback. The main results were validated on a robot. A distributed controller was used to obtain the fast control loops necessary for implementing the virtual muscles. The distributed control is demonstrated in an experiment where the robot splits into multiple functional parts. The five salamander behaviors were emulated by regulating the CPG with two descending drives. Reproducing the kinematics of backward stepping and struggling however required stronger muscle contractions. The passive oscillations observed in the salamander's tail during forward underwater stepping could be reproduced using a third descending drive of zero to the tail oscillators. This reduced the drag on the body in our hydrodynamic simulation. We explored the effect of local proprioceptive feedback during swimming and forward terrestrial stepping. We found that feedback could replace or reduce the need for different drives in both cases. It also reduced the variability of intersegmental phase lags toward values appropriate for locomotion. Our work suggests that different motor behaviors do not require different CPG circuits: a single circuit can produce various behaviors when modulated by descending drive and sensory feedback.

Project description:ObjectiveProprioceptive training is any intervention aiming to improve proprioceptive function with the ultimate goal to enhance motor function and performance. It has been promoted as an approach to enhance athletic performance and as a tool for sensorimotor rehabilitation. Numerous studies sought to provide evidence on the effectiveness of the approach. However, many different training regimes claiming to train proprioception report a variety of sensorimotor measures that are not directly comparable. This, in turn, makes it difficult to assess effectiveness across approaches. It is the objective of this study to systematically review recent empirical evidence to gain an understanding of which outcome measures are most sensitive, which populations may benefit most from proprioceptive training, and what are the effects on proprioceptive and motor systems.MethodsFour major databases were searched. The following inclusion criteria were applied: (1) A quantified pre- and post-treatment measure of proprioceptive function. (2) An intervention or training program believed to influence or enhance proprioceptive function. (3) Contained at least one form of treatment or outcome measure that is indicative of somatosensory function and not confounded by information from other sensory modalities. 4) The study reported of at least one quantified measure of motor performance.ResultsOf the 3,297 articles identified by the database search, 70 studies met the inclusion criteria and were included for further review. Across studies, proprioceptive training led to comparable gains in both proprioceptive (+46%) and motor performance (+45%). The majority of studies (50/70) applied active movement interventions. Interventions applying somatosensory stimulation were most successful in clinical populations. Joint position sense error (JPSE) was the most commonly used proprioceptive measure and presents a reliable and feasible measure for clinical use.ConclusionProprioceptive training can lead to significant improvements in proprioceptive and motor function across a range healthy and clinical populations. Regimens requiring active movement of the trainee tended to be most successful in improving sensorimotor performance. Conclusive evidence on how long training gains are retained is still lacking. There is no solid evidence about the underlying long-term neuroplastic changes associated proprioceptive training.

Dataset Information

Presynaptic gating of monkey proprioceptive signals for proper motor action.

Publications

Presynaptic gating of monkey proprioceptive signals for proper motor action.

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