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Centrally patterned rhythmic activity integrated by a peripheral circuit linking multiple oscillators

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Abstract

The central pattern generator for heartbeat in the medicinal leech, Hirudo generates rhythmic activity conveyed by heart excitor motor neurons in segments 3–18 to coordinate the bilateral tubular hearts and side vessels. We focus on behavior and the influence of previously un-described peripheral nerve circuitry. Extracellular recordings from the valve junction (VJ) where afferent vessels join the heart tube were combined with optical recording of contractions. Action potential bursts at VJs occurred in advance of heart tube and afferent vessel contractions. Transections of nerves were performed to reduce the output of the central pattern generator reaching the heart tube. Muscle contractions persisted but with a less regular rhythm despite normal central pattern generator rhythmicity. With no connections between the central pattern generator and heart tube, a much slower rhythm became manifest. Heart excitor neuron recordings showed that peripheral activity might contribute to the disruption of centrally entrained contractions. In the model presented, peripheral activity would normally modify the activity actually reaching the muscle. We also propose that the fundamental efferent unit is not a single heart excitor neuron, but rather is a functionally defined unit of about three adjacent motor neurons and the peripheral assembly of coupled peripheral oscillators.

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Abbreviations

AV:

Afferent vessel

ANR:

Anterior nerve root

CPG:

Central pattern generator

FMRFamide:

Phenylalanine-methionine-arginine-phenylalanine-NH2

HE:

Heart excitor

HT:

Heart tube

IPSP:

Inhibitory post-synaptic potential

Lav:

Latero-abdominal vessel

Ldv:

Latero-dorsal vessel

Llv:

Latero-lateral vessel

M:

Midbody segment

VJ:

Valve junction

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Acknowledgments

This work was funded in part by a Faculty Research and Creative Activities Award from Western Michigan University (J.J.) and a National Science Foundation REU award # DBI-1062883. We gratefully acknowledge the assistance of Michelle Alfert in helping gather and analyze preliminary data in intact animals and Wesley J. Thompson for his thoughtful insights on the data reported in this manuscript.

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  1. Department of Biological Sciences, Western Michigan University, Kalamazoo, MI, 49008, USA

    John Jellies & Daniel Kueh

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  1. John Jellies
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Correspondence to John Jellies.

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Jellies, J., Kueh, D. Centrally patterned rhythmic activity integrated by a peripheral circuit linking multiple oscillators. J Comp Physiol A 198, 567–582 (2012). https://doi.org/10.1007/s00359-012-0730-5

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