Cell
Volume 162, Issue 2, 16 July 2015, Pages 338-350
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Article
Primacy of Flexor Locomotor Pattern Revealed by Ancestral Reversion of Motor Neuron Identity

https://doi.org/10.1016/j.cell.2015.06.036Get rights and content
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Highlights

  • Motor neurons that innervate synergist muscles show synchronous locomotor firing

  • Flexor motor neurons activate in a sequence that matches target muscle positioning

  • Motor neuron columnar identity specifies locomotor firing pattern

  • Ancestral reversion of motor neuron identity reveals the primacy of flexor pattern

Summary

Spinal circuits can generate locomotor output in the absence of sensory or descending input, but the principles of locomotor circuit organization remain unclear. We sought insight into these principles by considering the elaboration of locomotor circuits across evolution. The identity of limb-innervating motor neurons was reverted to a state resembling that of motor neurons that direct undulatory swimming in primitive aquatic vertebrates, permitting assessment of the role of motor neuron identity in determining locomotor pattern. Two-photon imaging was coupled with spike inference to measure locomotor firing in hundreds of motor neurons in isolated mouse spinal cords. In wild-type preparations, we observed sequential recruitment of motor neurons innervating flexor muscles controlling progressively more distal joints. Strikingly, after reversion of motor neuron identity, virtually all firing patterns became distinctly flexor like. Our findings show that motor neuron identity directs locomotor circuit wiring and indicate the evolutionary primacy of flexor pattern generation.

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