Competition with primary sensory afferents drives remodeling of corticospinal axons in mature spinal motor circuits

Yu Qiu Jiang, Boubker Zaaimi, John H. Martin*

*Corresponding author for this work

Research output: Contribution to journalArticle

Abstract

Injury to the mature motor system drives significant spontaneous axonal sprouting instead of axon regeneration. Knowing the circuitlevel determinants of axonal sprouting is important for repairing motor circuits after injury to achieve functional rehabilitation. Competitive interactions are known to shape corticospinal tract axon outgrowth and withdrawal during development. Whether and how competition contributes to reorganization of mature spinal motor circuits is unclear. To study this question, we examined plastic changes in corticospinal axons in response to two complementary proprioceptive afferent manipulations: (1) enhancing proprioceptive afferents activity by electrical stimulation; or (2) diminishing their input by dorsal rootlet rhizotomy. Experiments were conducted in adult rats. Electrical stimulation produced proprioceptive afferent sprouting that was accompanied by significant corticospinal axon withdrawal and a decrease in corticospinal connections on cholinergic interneurons in the medial intermediate zone and C boutons on motoneurons. In contrast, dorsal rootlet rhizotomy led to a significant increase in corticospinal connections, including those on cholinergic interneurons; C bouton density increased correspondingly. Motor cortex-evoked muscle potentials showed parallel changes to those of corticospinal axons, suggesting that reciprocal corticospinal axon changes are functional. Using the two complementary models, we showed that competitive interactions between proprioceptive and corticospinal axons are an important determinant in the organization of mature corticospinal axons and spinal motor circuits. The activity- and synaptic space-dependent properties of the competition enables prediction of the remodeling of spared corticospinal connection and spinal motor circuits after injury and informs the target-specific control of corticospinal connections to promote functional recovery.

Original languageEnglish
Pages (from-to)193-203
Number of pages11
JournalJournal of Neuroscience
Volume36
Issue number1
DOIs
Publication statusPublished - 6 Jan 2016

Fingerprint

Axons
Rhizotomy
Interneurons
Cholinergic Agents
Electric Stimulation
Wounds and Injuries
Pyramidal Tracts
Motor Cortex
Motor Neurons
Evoked Potentials
Regeneration
Rehabilitation
Muscles

Bibliographical note

Copyright © 2016 the authors. Articles are released under a Creative Commons Attribution License after a 6 months embargo

Keywords

  • Activity dependent plasticity
  • Corticospinal tract
  • Motor cortex
  • Proprioceptive afferents
  • Rat

Cite this

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abstract = "Injury to the mature motor system drives significant spontaneous axonal sprouting instead of axon regeneration. Knowing the circuitlevel determinants of axonal sprouting is important for repairing motor circuits after injury to achieve functional rehabilitation. Competitive interactions are known to shape corticospinal tract axon outgrowth and withdrawal during development. Whether and how competition contributes to reorganization of mature spinal motor circuits is unclear. To study this question, we examined plastic changes in corticospinal axons in response to two complementary proprioceptive afferent manipulations: (1) enhancing proprioceptive afferents activity by electrical stimulation; or (2) diminishing their input by dorsal rootlet rhizotomy. Experiments were conducted in adult rats. Electrical stimulation produced proprioceptive afferent sprouting that was accompanied by significant corticospinal axon withdrawal and a decrease in corticospinal connections on cholinergic interneurons in the medial intermediate zone and C boutons on motoneurons. In contrast, dorsal rootlet rhizotomy led to a significant increase in corticospinal connections, including those on cholinergic interneurons; C bouton density increased correspondingly. Motor cortex-evoked muscle potentials showed parallel changes to those of corticospinal axons, suggesting that reciprocal corticospinal axon changes are functional. Using the two complementary models, we showed that competitive interactions between proprioceptive and corticospinal axons are an important determinant in the organization of mature corticospinal axons and spinal motor circuits. The activity- and synaptic space-dependent properties of the competition enables prediction of the remodeling of spared corticospinal connection and spinal motor circuits after injury and informs the target-specific control of corticospinal connections to promote functional recovery.",
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Competition with primary sensory afferents drives remodeling of corticospinal axons in mature spinal motor circuits. / Jiang, Yu Qiu; Zaaimi, Boubker; Martin, John H.

In: Journal of Neuroscience, Vol. 36, No. 1, 06.01.2016, p. 193-203.

Research output: Contribution to journalArticle

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