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The roles of ascending sensory signals and top-down central control in the entrainment of a locomotor CPG

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Abstract

Previous authors have proposed two basic hypotheses about the factors that form the basis of locomotor rhythms in walking insects: sensory feedback only or sensory feedback together with rhythmic activity of small neural circuits called central pattern generators (CPGs). Here we focus on the latter. Following this concept, to generate functional outputs, locomotor control must feature both rhythm generation by CPGs at the level of individual joints and coordination of their rhythmic activities, so that all muscles are activated in an appropriate pattern. This work provides an in-depth analysis of an aspect of this coordination process based on an existing network model of stick insect locomotion. Specifically, we consider how the control system for a single joint in the stick insect leg may produce rhythmic output when subjected to ascending sensory signals from other joints in the leg. In this work, the core rhythm generating CPG component of the joint under study is represented by a classical half-center oscillator constrained by a basic set of experimental observations. While the dynamical features of this CPG, including phase transitions by escape and release, are well understood, we provide novel insights about how these transition mechanisms yield entrainment to the incoming sensory signal, how entrainment can be lost under variation of signal strength and period or other perturbations, how entrainment can be restored by modulation of tonic top-down drive levels, and how these factors impact the duty cycle of the motor output.

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Acknowledgements

This work was partially supported by NSF DMS awards 1612913 and 1951095 (JR). SD gratefully acknowledges support from the German Research Foundation (DA1953/5-2).

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Authors and Affiliations

  1. Department of Mathematics, University of Pittsburgh, Pittsburgh, PA, USA

    Marcello G. Codianni & Jonathan E. Rubin

  2. Institute of Neuroscience and Medicine - Cognitive Neuroscience, Institute of Zoology, Forschungszentrum Jülich and University of Cologne, Cologne, Germany

    Silvia Daun

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  1. Marcello G. Codianni
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  2. Silvia Daun
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Correspondence to Jonathan E. Rubin.

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Communicated by Benjamin Lindner.

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Codianni, M.G., Daun, S. & Rubin, J.E. The roles of ascending sensory signals and top-down central control in the entrainment of a locomotor CPG. Biol Cybern 114, 533–555 (2020). https://doi.org/10.1007/s00422-020-00852-8

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