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Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion

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Abstract

Locomotion is produced by a central pattern generator. Its spinal cord organization is generally considered to be distributed, with more rhythmogenic rostral lumbar segments. While this produces a rostrocaudally traveling wave in undulating species, this is not thought to occur in limbed vertebrates, with the exception of the interneuronal traveling wave demonstrated in fictive cat scratching (Cuellar et al. J Neurosci 29:798–810, 2009). Here, we reexamine this hypothesis in the frog, using the seven muscle synergies A to G previously identified with intraspinal NMDA (Saltiel et al. J Neurophysiol 85:605–619, 2001). We find that locomotion consists of a sequence of synergy activations (A–B–G–A–F–E–G). The same sequence is observed when focal NMDA iontophoresis in the spinal cord elicits a caudal extension-lateral force-flexion cycle (flexion onset without the C synergy). Examining the early NMDA-evoked motor output at 110 sites reveals a rostrocaudal topographic organization of synergy encoding by the lumbar cord. Each synergy is preferentially activated from distinct regions, which may be multiple, and partially overlap between different synergies. Comparing the sequence of synergy activation in locomotion with their spinal cord topography suggests that the locomotor output is achieved by a rostrocaudally traveling wave of activation in the swing–stance cycle. A two-layer circuitry model, based on this topography and a traveling wave reproduces this output and explores its possible modifications under different afferent inputs. Our results and simulations suggest that a rostrocaudally traveling wave of excitation takes advantage of the topography of interneuronal regions encoding synergies, to activate them in the proper sequence for locomotion.

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Acknowledgments

This work was supported by NIH grant NS 09343 to Emilio Bizzi, and the Swiss National Science Foundation to Kuno Wyler-Duda. We would like to thank Vincent Cheung and Serge Rossignol for their helpful reading of the manuscript, Margo Cantor and Sylvester Szczepanowski for technical support, and Charlotte Potak for administrative assistance.

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Authors and Affiliations

  1. Department of Brain and Cognitive Sciences, McGovern Institute for Brain Research, Massachusetts Institute of Technology, 77 Massachusetts Ave. 46-6189, Cambridge, MA, 02139, USA

    Philippe Saltiel, Andrea d’Avella, Kuno Wyler-Duda & Emilio Bizzi

  2. Department of Biomedical Sciences and Morphological and Functional Images, University of Messina, Messina, Italy

    Andrea d’Avella

  3. Laboratory of Neuromotor Physiology, Santa Lucia Foundation, Rome, Italy

    Andrea d’Avella

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  1. Philippe Saltiel
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  2. Andrea d’Avella
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Correspondence to Philippe Saltiel.

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Saltiel, P., d’Avella, A., Wyler-Duda, K. et al. Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion. Brain Struct Funct 221, 3869–3890 (2016). https://doi.org/10.1007/s00429-015-1133-5

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