Specificity of Monosynaptic Sensory-Motor Connections Imposed by Repellent Sema3E-PlexinD1 Signaling
Kaori Fukuhara,
Fumiyasu Imai,
David R. Ladle,
Kei-ichi Katayama,
Jennifer R. Leslie,
Silvia Arber,
Thomas M. Jessell,
Yutaka Yoshida
Affiliations
Kaori Fukuhara
Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA
Fumiyasu Imai
Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA
David R. Ladle
Department of Neuroscience, Cell Biology, and Physiology, Wright State University, Dayton, OH 45435, USA
Kei-ichi Katayama
Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA
Jennifer R. Leslie
Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA
Silvia Arber
Biozentrum, Department of Cell Biology, University of Basel, 4056 Basel, Switzerland
Thomas M. Jessell
Howard Hughes Medical Institute, Departments of Neuroscience and Biochemistry and Molecular Biophysics, Kavli Institute for Brain Science, Columbia University, New York, NY 10032, USA
Yutaka Yoshida
Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA
In mammalian spinal cord, group Ia proprioceptive afferents form selective monosynaptic connections with a select group of motor pool targets. The extent to which sensory recognition of motor neurons contributes to the selectivity of sensory-motor connections remains unclear. We show here that proprioceptive sensory afferents that express PlexinD1 avoid forming monosynaptic connections with neurons in Sema3E+ motor pools yet are able to form direct connections with neurons in Sema3Eoff motor pools. Anatomical and electrophysiological analysis of mice in which Sema3E-PlexinD1 signaling has been deregulated or inactivated genetically reveals that repellent signaling underlies aspects of the specificity of monosynaptic sensory-motor connectivity in these reflex arcs. A semaphorin-based system of motor neuron recognition and repulsion therefore contributes to the formation of specific sensory-motor connections in mammalian spinal cord.
