Functional recovery of a locomotor network after injury: plasticity beyond the central nervous system

Joshua G. Puhl, Anthony W. Bigelow, Mara C.P. Rue, Karen A. Mesce

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4 Scopus citations

Abstract

Many animals depend on descending information from the brain for the initiation and proper execution of locomotion. Interestingly, after injury and the loss of such inputs, locomotor function can sometimes be regained without the regrowth of central connections. In the medicinal leech, Hirudo verbana, we have shown that crawling reemerges after removal of descending inputs. Here, we studied the mechanisms underlying this return of locomotion by asking if central pattern generators (CPGs) in crawl-recovered leeches are sufficient to produce crawl-specific intersegmental coordination. From recovered animals, we treated isolated chains of ganglia with dopamine to activate the crawl CPGs (one crawl CPG per ganglion) and observed fictive crawl-like bursting in the dorsal-longitudinal-excitor motoneuron (DE-3), an established crawl-monitor neuron. However, these preparations did not exhibit crawl-specific coordination across the CPGs. Although the crawl CPGs always generated bidirectional activation of adjacent CPGs, we never observed crawl-appropriate intersegmental phase delays. Because central circuits alone were unable to organize crawl-specific coordination, we tested the coordinating role of the peripheral nervous system. In transected leeches normally destined for recovery, we removed afferent information to the anterior-most (lead) ganglion located below the nerve-cord transection site. In these dually treated animals, overt crawling was greatly delayed or prevented. After filling the peripheral nerves with Neurobiotin tracer distal to the nerve-root lesion, we found a perfect correlation between regrowth of peripheral neuronal fibers and crawl recovery. Our study establishes that during recovery after injury, crawl-specific intersegmental coordination switches to a new dependence on afferent information.

Original languageEnglish (US)
Article numbere0195-18.2018
JournaleNeuro
Volume5
Issue number4
DOIs
StatePublished - Jul 1 2018

Bibliographical note

Funding Information:
This work was supported by a grant IOS-1454904 to KAM from the National Science Foundation. *Authors contributed equally to this work and are thus first co-authors. A.W. Bigelow’s present address is Graduate Program in Neuroscience, University of Washington, Seattle, WA 98105, USA. M.C.P. Rue’s present address is Volen Center and Biology Department, Brandeis University, Waltham, MA 02454, USA. Correspondence should be addressed to Karen A. Mesce, Department of Entomology, 219 Hodson Hall, 1980 Folwell Ave., St. Paul, MN, 55108. E-mail: mesce001@umn.edu. DOI:http://dx.doi.org/10.1523/ENEURO.0195-18.2018 Copyright © 2018 Puhl et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

Funding Information:
This work was supported by a grant IOS-1454904 to KAM from the National Science Foundation.

Publisher Copyright:
© 2018 Puhl et al.

Keywords

  • CPG
  • Crawling
  • Dopamine
  • Homeostatic plasticity
  • Locomotion
  • Spinal cord injury

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