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Treatment with Riluzole Restores Normal Control of Soleus and Extensor Digitorum Longus Muscles during Locomotion in Adult Rats after Sciatic Nerve Crush at Birth

1 , * , 1 , 2 , 2

PLoS ONE

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      Abstract

      The effects of sciatic nerve crush (SNC) and treatment with Riluzole on muscle activity during unrestrained locomotion were identified in an animal model by analysis of the EMG activity recorded from soleus (Sol) and extensor digitorum longus (EDL) muscles of both hindlimbs; in intact rats (IN) and in groups of rats treated for 14 days with saline (S) or Riluzole (R) after right limb nerve crush at the 1 st (1S and 1R) or 2 nd (2S and 2R) day after birth. Changes in the locomotor pattern of EMG activity were correlated with the numbers of survived motor units (MUs) identified in investigated muscles. S rats with 2–8 and 10–28 MUs that survived in Sol and EDL muscles respectively showed increases in the duration and duty factor of muscle EMG activity and a loss of correlation between the duty factors of muscle activity, and abnormal flexor-extensor co-activation 3 months after SNC. R rats with 5, 6 (Sol) and 15–29 MUs (EDL) developed almost normal EMG activity of both Sol and control EDL muscles, whereas EDL muscles with SNC showed a lack of recovery. R rats with 8 (Sol) and 23–33 (EDL) MUs developed almost normal EMG activities of all four muscles. A subgroup of S rats with a lack of recovery and R rats with almost complete recovery that had similar number of MUs (8 and 24–28 vs 8 and 23–26), showed that the number of MUs was not the only determinant of treatment effectiveness. The results demonstrated that rats with SNC failed to develop normal muscle activity due to malfunction of neuronal circuits attenuating EDL muscle activity during the stance phase, whereas treatment with Riluzole enabled almost normal EMG activity of Sol and EDL muscles during locomotor movement.

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      Dynamic sensorimotor interactions in locomotion.

      Locomotion results from intricate dynamic interactions between a central program and feedback mechanisms. The central program relies fundamentally on a genetically determined spinal circuitry (central pattern generator) capable of generating the basic locomotor pattern and on various descending pathways that can trigger, stop, and steer locomotion. The feedback originates from muscles and skin afferents as well as from special senses (vision, audition, vestibular) and dynamically adapts the locomotor pattern to the requirements of the environment. The dynamic interactions are ensured by modulating transmission in locomotor pathways in a state- and phase-dependent manner. For instance, proprioceptive inputs from extensors can, during stance, adjust the timing and amplitude of muscle activities of the limbs to the speed of locomotion but be silenced during the opposite phase of the cycle. Similarly, skin afferents participate predominantly in the correction of limb and foot placement during stance on uneven terrain, but skin stimuli can evoke different types of responses depending on when they occur within the step cycle. Similarly, stimulation of descending pathways may affect the locomotor pattern in only certain phases of the step cycle. Section ii reviews dynamic sensorimotor interactions mainly through spinal pathways. Section iii describes how similar sensory inputs from the spinal or supraspinal levels can modify locomotion through descending pathways. The sensorimotor interactions occur obviously at several levels of the nervous system. Section iv summarizes presynaptic, interneuronal, and motoneuronal mechanisms that are common at these various levels. Together these mechanisms contribute to the continuous dynamic adjustment of sensorimotor interactions, ensuring that the central program and feedback mechanisms are congruous during locomotion.
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        Organization of mammalian locomotor rhythm and pattern generation.

        Central pattern generators (CPGs) located in the spinal cord produce the coordinated activation of flexor and extensor motoneurons during locomotion. Previously proposed architectures for the spinal locomotor CPG have included the classical half-center oscillator and the unit burst generator (UBG) comprised of multiple coupled oscillators. We have recently proposed another organization in which a two-level CPG has a common rhythm generator (RG) that controls the operation of the pattern formation (PF) circuitry responsible for motoneuron activation. These architectures are discussed in relation to recent data obtained during fictive locomotion in the decerebrate cat. The data show that the CPG can maintain the period and phase of locomotor oscillations both during spontaneous deletions of motoneuron activity and during sensory stimulation affecting motoneuron activity throughout the limb. The proposed two-level CPG organization has been investigated with a computational model which incorporates interactions between the CPG, spinal circuits and afferent inputs. The model includes interacting populations of spinal interneurons and motoneurons modeled in the Hodgkin-Huxley style. Our simulations demonstrate that a relatively simple CPG with separate RG and PF networks can realistically reproduce many experimental phenomena including spontaneous deletions of motoneuron activity and a variety of effects of afferent stimulation. The model suggests plausible explanations for a number of features of real CPG operation that would be difficult to explain in the framework of the classical single-level CPG organization. Some modeling predictions and directions for further studies of locomotor CPG organization are discussed.
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          Outcome measures of peripheral nerve regeneration.

          Animal models of nerve compression, crush, and transection injuries of peripheral nerves have been subject to extensive study in order to understand the mechanisms of injury and axon regeneration and to investigate methods to promote axon regeneration and improve functional outcomes following nerve injury. Six outcome measures of regenerative success including axon and neuron counts, muscle and motor unit contractile forces, and behavior are reviewed in the context of nerve injury types, crush, transection and nerve repair by direct coaptation, or transection and repair via a nerve graft or conduit. The measures are evaluated for sciatic, tibial, common peroneal, femoral, single nerve branches such as the soleus nerve, and facial nerves. Their validity is discussed in the context of study objectives and the nerve branch. The case is made that outcome measures of axon counts and muscle contractile forces may be valid during the early phases of axon regeneration when regenerating sprouts emerge asynchronously from the proximal nerve stump and regenerate towards their denervated targets. However, care must be taken especially when experimental interventions differentially affect how many neurons regenerate axons and the number of axons per neuron that sprout from the proximal nerve stumps. Examples of erroneous conclusions are given to illustrate the need for researchers to ensure that the appropriate outcome measures are used in the evaluation of the success of peripheral nerve regeneration. Copyright © 2011 Elsevier GmbH. All rights reserved.
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            Author and article information

            Affiliations
            [1 ]Department of Engineering of Nervous and Muscular System, Nałęcz Institute of Biocybernetics and Biomedical Engineering, PAS, Warsaw, Poland
            [2 ]Department of Neurophysiology, Nencki Institute of Experimental Biology, PAS, Warsaw, Poland
            Szegedi Tudomanyegyetem, HUNGARY
            Author notes

            Competing Interests: The authors have declared that no competing interests exist.

            • Conceptualization: WZ AMC US.

            • Formal analysis: WZ.

            • Investigation: AMC US.

            • Methodology: WZ AMC US.

            • Supervision: WZ AMC.

            • Visualization: WZ.

            • Writing – original draft: WZ AMC US.

            Contributors
            Role: Editor
            Journal
            PLoS One
            PLoS ONE
            plos
            plosone
            PLoS ONE
            Public Library of Science (San Francisco, CA USA )
            1932-6203
            17 January 2017
            2017
            : 12
            : 1
            28095499
            5240973
            10.1371/journal.pone.0170235
            PONE-D-16-40363
            (Editor)
            © 2017 Zmysłowski et al

            This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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            Figures: 11, Tables: 1, Pages: 28
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            Funding
            This work was supported by grants from the Polish Ministry of Science and High Education 1527/PO1/2006/31 and statutory donation from the Nencki Institute as well as the Nałęcz Institute.
            Categories
            Research Article
            Research and Analysis Methods
            Bioassays and Physiological Analysis
            Electrophysiological Techniques
            Muscle Electrophysiology
            Electromyography
            Biology and Life Sciences
            Biomechanics
            Biological Locomotion
            Biology and Life Sciences
            Physiology
            Biological Locomotion
            Medicine and Health Sciences
            Physiology
            Biological Locomotion
            Biology and Life Sciences
            Anatomy
            Nervous System
            Neuroanatomy
            Neural Pathways
            Medicine and Health Sciences
            Anatomy
            Nervous System
            Neuroanatomy
            Neural Pathways
            Biology and Life Sciences
            Neuroscience
            Neuroanatomy
            Neural Pathways
            Biology and Life Sciences
            Anatomy
            Nervous System
            Nerves
            Sciatic Nerves
            Medicine and Health Sciences
            Anatomy
            Nervous System
            Nerves
            Sciatic Nerves
            Research and Analysis Methods
            Bioassays and Physiological Analysis
            Muscle Analysis
            Biology and Life Sciences
            Anatomy
            Musculoskeletal System
            Medicine and Health Sciences
            Anatomy
            Musculoskeletal System
            Biology and Life Sciences
            Anatomy
            Musculoskeletal System
            Muscles
            Soleus Muscles
            Medicine and Health Sciences
            Anatomy
            Musculoskeletal System
            Muscles
            Soleus Muscles
            Medicine and Health Sciences
            Critical Care and Emergency Medicine
            Trauma Medicine
            Traumatic Injury
            Musculoskeletal Injury
            Custom metadata
            All relevant data are within the paper and its Supporting Information files.

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