The Ancient Origins of Neural Substrates for Land Walking

Heekyung Jung, Myungin Baek, Kristen P. D'Elia, Catherine Boisvert, Peter D. Currie, Boon Hui Tay, Byrappa Venkatesh, Stuart M. Brown, Adriana Heguy, David Schoppik, Jeremy S. Dasen

Research output: Contribution to journalArticleResearchpeer-review

27 Citations (Scopus)

Abstract

Walking is the predominant locomotor behavior expressed by land-dwelling vertebrates, but it is unknown when the neural circuits that are essential for limb control first appeared. Certain fish species display walking-like behaviors, raising the possibility that the underlying circuitry originated in primitive marine vertebrates. We show that the neural substrates of bipedalism are present in the little skate Leucoraja erinacea, whose common ancestor with tetrapods existed ∼420 million years ago. Leucoraja exhibits core features of tetrapod locomotor gaits, including left-right alternation and reciprocal extension-flexion of the pelvic fins. Leucoraja also deploys a remarkably conserved Hox transcription factor-dependent program that is essential for selective innervation of fin/limb muscle. This network encodes peripheral connectivity modules that are distinct from those used in axial muscle-based swimming and has apparently been diminished in most modern fish. These findings indicate that the circuits that are essential for walking evolved through adaptation of a genetic regulatory network shared by all vertebrates with paired appendages. Video Abstract: The circuits involved in limb control were established in the common ancestor to all vertebrates with pair appendages millions of years before the first tetrapod walked on land.

Original languageEnglish
Pages (from-to)667-682
Number of pages16
JournalCell
Volume172
Issue number4
DOIs
Publication statusPublished - 8 Feb 2018

Keywords

  • development
  • evolution
  • Hox gene
  • locomotion
  • motor neuron
  • neural circuit
  • spinal cord

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