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      A Neuro-Mechanical Model Explaining the Physiological Role of Fast and Slow Muscle Fibres at Stop and Start of Stepping of an Insect Leg

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          Abstract

          Stop and start of stepping are two basic actions of the musculo-skeletal system of a leg. Although they are basic phenomena, they require the coordinated activities of the leg muscles. However, little is known of the details of how these activities are generated by the interactions between the local neuronal networks controlling the fast and slow muscle fibres at the individual leg joints. In the present work, we aim at uncovering some of those details using a suitable neuro-mechanical model. It is an extension of the model in the accompanying paper and now includes all three antagonistic muscle pairs of the main joints of an insect leg, together with their dedicated neuronal control, as well as common inhibitory motoneurons and the residual stiffness of the slow muscles. This model enabled us to study putative processes of intra-leg coordination during stop and start of stepping. We also made use of the effects of sensory signals encoding the position and velocity of the leg joints. Where experimental observations are available, the corresponding simulation results are in good agreement with them. Our model makes detailed predictions as to the coordination processes of the individual muscle systems both at stop and start of stepping. In particular, it reveals a possible role of the slow muscle fibres at stop in accelerating the convergence of the leg to its steady-state position. These findings lend our model physiological relevance and can therefore be used to elucidate details of the stop and start of stepping in insects, and perhaps in other animals, too.

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          Most cited references 18

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          Neural control of unloaded leg posture and of leg swing in stick insect, cockroach, and mouse differs from that in larger animals.

           Scott L Hooper (corresponding) ,  Christoph Guschlbauer,  Marcus Blümel (2009)
          Stick insect (Carausius morosus) leg muscles contract and relax slowly. Control of stick insect leg posture and movement could therefore differ from that in animals with faster muscles. Consistent with this possibility, stick insect legs maintained constant posture without leg motor nerve activity when the animals were rotated in air. That unloaded leg posture was an intrinsic property of the legs was confirmed by showing that isolated legs had constant, gravity-independent postures. Muscle ablation experiments, experiments showing that leg muscle passive forces were large compared with gravitational forces, and experiments showing that, at the rest postures, agonist and antagonist muscles generated equal forces indicated that these postures depended in part on leg muscles. Leg muscle recordings showed that stick insect swing motor neurons fired throughout the entirety of swing. To test whether these results were specific to stick insect, we repeated some of these experiments in cockroach (Periplaneta americana) and mouse. Isolated cockroach legs also had gravity-independent rest positions and mouse swing motor neurons also fired throughout the entirety of swing. These data differ from those in human and horse but not cat. These size-dependent variations in whether legs have constant, gravity-independent postures, in whether swing motor neurons fire throughout the entirety of swing, and calculations of how quickly passive muscle force would slow limb movement as limb size varies suggest that these differences may be caused by scaling. Limb size may thus be as great a determinant as phylogenetic position of unloaded limb motor control strategy.
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            A neuromechanical model explaining forward and backward stepping in the stick insect.

            The mechanism underlying the generation of stepping has been the object of intensive studies. Stepping involves the coordinated movement of different leg joints and is, in the case of insects, produced by antagonistic muscle pairs. In the stick insect, the coordinated actions of three such antagonistic muscle pairs produce leg movements and determine the stepping pattern of the limb. The activity of the muscles is controlled by the nervous system as a whole and more specifically by local neuronal networks for each muscle pair. While many basic properties of these control mechanisms have been uncovered, some important details of their interactions in various physiological conditions have so far remained unknown. In this study, we present a neuromechanical model of the coupled protractor-retractor and levator-depressor neuromuscular systems and use it to elucidate details of their coordinated actions during forward and backward walking. The switch from protraction to retraction is evoked at a critical angle of the femur during downward movement. This angle represents a sensory input that integrates load, motion, and ground contact. Using the model, we can make detailed suggestions as to how rhythmic stepping might be generated by the central pattern generators of the local neuronal networks, how this activity might be transmitted to the corresponding motoneurons, and how the latter might control the activity of the related muscles. The entirety of these processes yields the coordinated interaction between neuronal and mechanical parts of the system. Moreover, we put forward a mechanism by which motoneuron activity could be modified by a premotor network and suggest that this mechanism might serve as a basis for fast adaptive behavior, like switches between forward and backward stepping, which occur, for example, during curve walking, and especially sharp turning, of insects.
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              Role of local nonspiking interneurons in the generation of rhythmic motor activity in the stick insect.

              Local nonspiking interneurons in the thoracic ganglia of insects are important premotor elements in posture control and locomotion. It was investigated whether these interneurons are involved in the central neuronal circuits generating the oscillatory motor output of the leg muscle system during rhythmic motor activity. Intracellular recordings from premotor nonspiking interneurons were made in the isolated and completely deafferented mesothoracic ganglion of the stick insect in preparations exhibiting rhythmic motor activity induced by the muscarinic agonist pilocarpine. All interneurons investigated provided synaptic drive to one or more motoneuron pools supplying the three proximal leg joints, that is, the thoraco-coxal joint, the coxa-trochanteral joint and the femur-tibia joint. During rhythmicity in 83% (n = 67) of the recorded interneurons, three different kinds of synaptic oscillations in membrane potential were observed: (1) Oscillations were closely correlated with the activity of motoneuron pools affected; (2) membrane potential oscillations reflected only certain aspects of motoneuronal rhythmicity; and (3) membrane potential oscillations were correlated mainly with the occurrence of spontaneous recurrent patterns (SRP) of activity in the motoneuron pools. In individual interneurons membrane potential oscillations were associated with phase-dependent changes in the neuron's membrane conductance. Artificial changes in the interneurons' membrane potential strongly influenced motor activity. Injecting current pulses into individual interneurons caused a reset of rhythmicity in motoneurons. Furthermore, current injection into interneurons influenced shape and probability of occurrence for SRPs. Among others, identified nonspiking interneurons that are involved in posture control of leg joints were found to exhibit the above properties. From these results, the following conclusions on the role of nonspiking interneurons in the generation of rhythmic motor activity, and thus potentially also during locomotion, emerge: (1) During rhythmic motor activity most nonspiking interneurons receive strong synaptic drive from central rhythm-generating networks; and (2) individual nonspiking interneurons some of which underlie sensory-motor pathways in posture control, are elements of central neuronal networks that generate alternating activity in antagonistic leg motoneuron pools.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                22 November 2013
                : 8
                : 11
                Affiliations
                [1 ]Emmy Noether Research Group of Computational Biology, Department of Animal Physiology, University of Cologne, Cologne, Germany
                [2 ]Department of Animal Physiology, University of Cologne, Cologne, Germany
                Mount Sinai School of Medicine, United States of America
                Author notes

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

                Conceived and designed the experiments: TT SDG. Performed the experiments: TT MG. Analyzed the data: TT MG JS AB SDG. Contributed reagents/materials/analysis tools: AB SDG. Wrote the paper: TT MG JS AB SDG.

                Article
                PONE-D-13-17636
                10.1371/journal.pone.0078246
                3838373

                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.

                Page count
                Pages: 14
                Funding
                This work was supported by DFG Emmy-Noether Programme ( http://www.dfg.de/en/research_funding/programmes/individual/emmy_noether/index.html). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Research Article

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