A Gradient in Synaptic Strength and Plasticity among Motoneurons Provides a Peripheral Mechanism for Locomotor Control

Wei Chun Wang, Paul Brehm

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

The recruitment of motoneurons during force generation follows a general pattern that has been confirmed across diverse species [1–3]. Motoneurons are recruited systematically according to synaptic inputs and intrinsic cellular properties and corresponding to movements of different intensities. However, much less is known about the output properties of individual motoneurons and how they affect the translation of motoneuron recruitment to the strength of muscle contractions. In larval zebrafish, spinal motoneurons are recruited in a topographic gradient according to their input resistance (Rin) at different swimming strengths and speeds. Whereas dorsal, lower-Rin primary motoneurons (PMns) are only activated during behaviors that involve strong and fast body bends, more ventral, higher-Rin secondary motoneurons (SMns) are recruited during weaker and slower movements [4–6]. Here we perform in vivo paired recordings between identified spinal motoneurons and skeletal muscle cells in larval zebrafish. We characterize individual motoneuron outputs to single muscle cells and show that the strength and reliability of motoneuron outputs are inversely correlated with motoneuron Rin. During repetitive high-frequency motoneuron drive, PMn synapses undergo depression, whereas SMn synapses potentiate. We monitor muscle cell contractions elicited by single motoneurons and show that the pattern of motoneuron output strength and plasticity observed in electrophysiological recordings is reflected in muscle shortening. Our findings indicate a link between the recruitment pattern and output properties of spinal motoneurons that can together generate appropriate intensities for muscle contractions. We demonstrate that motoneuron output properties provide an additional peripheral mechanism for graded locomotor control at the neuromuscular junction.

Original languageEnglish (US)
Pages (from-to)415-422
Number of pages8
JournalCurrent Biology
Volume27
Issue number3
DOIs
StatePublished - Feb 6 2017

Fingerprint

Neuronal Plasticity
Motor Neurons
motor neurons
Plasticity
Muscle
Cells
Muscle Contraction
myocytes
Muscle Cells
muscle contraction
Zebrafish
synapse
Danio rerio
Synapses
Neuromuscular Junction

Keywords

  • input resistance
  • intrinsic cellular property
  • locomotion
  • motor neuron
  • neuromuscular junction
  • skeletal muscle
  • spinal cord
  • zebrafish

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

A Gradient in Synaptic Strength and Plasticity among Motoneurons Provides a Peripheral Mechanism for Locomotor Control. / Wang, Wei Chun; Brehm, Paul.

In: Current Biology, Vol. 27, No. 3, 06.02.2017, p. 415-422.

Research output: Contribution to journalArticle

@article{2772d5d8aac64e998b9195c03b807f57,
title = "A Gradient in Synaptic Strength and Plasticity among Motoneurons Provides a Peripheral Mechanism for Locomotor Control",
abstract = "The recruitment of motoneurons during force generation follows a general pattern that has been confirmed across diverse species [1–3]. Motoneurons are recruited systematically according to synaptic inputs and intrinsic cellular properties and corresponding to movements of different intensities. However, much less is known about the output properties of individual motoneurons and how they affect the translation of motoneuron recruitment to the strength of muscle contractions. In larval zebrafish, spinal motoneurons are recruited in a topographic gradient according to their input resistance (Rin) at different swimming strengths and speeds. Whereas dorsal, lower-Rin primary motoneurons (PMns) are only activated during behaviors that involve strong and fast body bends, more ventral, higher-Rin secondary motoneurons (SMns) are recruited during weaker and slower movements [4–6]. Here we perform in vivo paired recordings between identified spinal motoneurons and skeletal muscle cells in larval zebrafish. We characterize individual motoneuron outputs to single muscle cells and show that the strength and reliability of motoneuron outputs are inversely correlated with motoneuron Rin. During repetitive high-frequency motoneuron drive, PMn synapses undergo depression, whereas SMn synapses potentiate. We monitor muscle cell contractions elicited by single motoneurons and show that the pattern of motoneuron output strength and plasticity observed in electrophysiological recordings is reflected in muscle shortening. Our findings indicate a link between the recruitment pattern and output properties of spinal motoneurons that can together generate appropriate intensities for muscle contractions. We demonstrate that motoneuron output properties provide an additional peripheral mechanism for graded locomotor control at the neuromuscular junction.",
keywords = "input resistance, intrinsic cellular property, locomotion, motor neuron, neuromuscular junction, skeletal muscle, spinal cord, zebrafish",
author = "Wang, {Wei Chun} and Paul Brehm",
year = "2017",
month = "2",
day = "6",
doi = "10.1016/j.cub.2016.12.010",
language = "English (US)",
volume = "27",
pages = "415--422",
journal = "Current Biology",
issn = "0960-9822",
publisher = "Cell Press",
number = "3",

}

TY - JOUR

T1 - A Gradient in Synaptic Strength and Plasticity among Motoneurons Provides a Peripheral Mechanism for Locomotor Control

AU - Wang, Wei Chun

AU - Brehm, Paul

PY - 2017/2/6

Y1 - 2017/2/6

N2 - The recruitment of motoneurons during force generation follows a general pattern that has been confirmed across diverse species [1–3]. Motoneurons are recruited systematically according to synaptic inputs and intrinsic cellular properties and corresponding to movements of different intensities. However, much less is known about the output properties of individual motoneurons and how they affect the translation of motoneuron recruitment to the strength of muscle contractions. In larval zebrafish, spinal motoneurons are recruited in a topographic gradient according to their input resistance (Rin) at different swimming strengths and speeds. Whereas dorsal, lower-Rin primary motoneurons (PMns) are only activated during behaviors that involve strong and fast body bends, more ventral, higher-Rin secondary motoneurons (SMns) are recruited during weaker and slower movements [4–6]. Here we perform in vivo paired recordings between identified spinal motoneurons and skeletal muscle cells in larval zebrafish. We characterize individual motoneuron outputs to single muscle cells and show that the strength and reliability of motoneuron outputs are inversely correlated with motoneuron Rin. During repetitive high-frequency motoneuron drive, PMn synapses undergo depression, whereas SMn synapses potentiate. We monitor muscle cell contractions elicited by single motoneurons and show that the pattern of motoneuron output strength and plasticity observed in electrophysiological recordings is reflected in muscle shortening. Our findings indicate a link between the recruitment pattern and output properties of spinal motoneurons that can together generate appropriate intensities for muscle contractions. We demonstrate that motoneuron output properties provide an additional peripheral mechanism for graded locomotor control at the neuromuscular junction.

AB - The recruitment of motoneurons during force generation follows a general pattern that has been confirmed across diverse species [1–3]. Motoneurons are recruited systematically according to synaptic inputs and intrinsic cellular properties and corresponding to movements of different intensities. However, much less is known about the output properties of individual motoneurons and how they affect the translation of motoneuron recruitment to the strength of muscle contractions. In larval zebrafish, spinal motoneurons are recruited in a topographic gradient according to their input resistance (Rin) at different swimming strengths and speeds. Whereas dorsal, lower-Rin primary motoneurons (PMns) are only activated during behaviors that involve strong and fast body bends, more ventral, higher-Rin secondary motoneurons (SMns) are recruited during weaker and slower movements [4–6]. Here we perform in vivo paired recordings between identified spinal motoneurons and skeletal muscle cells in larval zebrafish. We characterize individual motoneuron outputs to single muscle cells and show that the strength and reliability of motoneuron outputs are inversely correlated with motoneuron Rin. During repetitive high-frequency motoneuron drive, PMn synapses undergo depression, whereas SMn synapses potentiate. We monitor muscle cell contractions elicited by single motoneurons and show that the pattern of motoneuron output strength and plasticity observed in electrophysiological recordings is reflected in muscle shortening. Our findings indicate a link between the recruitment pattern and output properties of spinal motoneurons that can together generate appropriate intensities for muscle contractions. We demonstrate that motoneuron output properties provide an additional peripheral mechanism for graded locomotor control at the neuromuscular junction.

KW - input resistance

KW - intrinsic cellular property

KW - locomotion

KW - motor neuron

KW - neuromuscular junction

KW - skeletal muscle

KW - spinal cord

KW - zebrafish

UR - http://www.scopus.com/inward/record.url?scp=85009786113&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85009786113&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2016.12.010

DO - 10.1016/j.cub.2016.12.010

M3 - Article

VL - 27

SP - 415

EP - 422

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 3

ER -