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Characterization of the encoding properties of intraspinal mechanosensory neurons in the lamprey

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Abstract

Proprioceptive sensory inputs are an integral part of the closed-loop system of locomotion. In the lamprey, a model organism for vertebrate locomotion, such sensory inputs come from intraspinal mechanosensory cells called “edge cells”. These edge cells synapse directly onto interneurons in the spinal central pattern generator (CPG) circuit and allow the CPG to adjust the motor output according to how the body is bending. However, the encoding properties of the edge cells have never been fully characterized. To identify these properties and better understand edge cells’ role in locomotion, we isolated spinal cords of silver lampreys (Ichthyomyzon unicuspis) and recorded extracellularly from the lateral tracts where edge cell axons are located. We identified cells that responded to mechanical stimuli and used standard spike sorting algorithms to identify separate units, then examined how the cells respond to bending rate and bending angle. Although some cells respond to the bending angle, as was previously known, the strongest and most common responses were to bending velocity. These encoding properties will help us better understand how lampreys and other basal vertebrates adapt their locomotor rhythms to different water flow patterns, perturbations, or other unexpected changes in their environments.

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Abbreviations

ANOVA:

Analysis of variance

CPG:

Central pattern generator

K–S:

Kolmogorov–Smirnov test for identical distributions

PCA:

Principal component analysis

PD:

Proportional-derivative

PID:

Proportional-integral-derivative

CL:

Center to left

LC:

Left to center

LL:

Hold on left side

CR:

Center to right

RC:

Right to center

RR:

Hold on right side

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Acknowledgements

This study benefited from discussions with Avis H. Cohen, Lisa J. Fauci, Christina Hamlet, and Megan C. Leftwich. Funding support was received from the National Science Foundation under Grant DBI-RCN 1325165 (to L. J. Fauci and A. H. Cohen). This material is based upon work supported by, or in part by, the US Army Research Laboratory and the US Army Research Office under Contract/Grant No. W911NF-14-1-0268. All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the Tufts University animal care and use committee.

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Authors and Affiliations

  1. University of Maryland Baltimore County, Baltimore, USA

    Nicole Massarelli & Kathleen A. Hoffman

  2. Tufts University, Medford, USA

    Allan L. Yau & Eric D. Tytell

  3. University of Maryland, College Park, USA

    Tim Kiemel

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  1. Nicole Massarelli
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  2. Allan L. Yau
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  3. Kathleen A. Hoffman
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  4. Tim Kiemel
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  5. Eric D. Tytell
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Correspondence to Eric D. Tytell.

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Massarelli, N., Yau, A.L., Hoffman, K.A. et al. Characterization of the encoding properties of intraspinal mechanosensory neurons in the lamprey. J Comp Physiol A 203, 831–841 (2017). https://doi.org/10.1007/s00359-017-1196-2

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