Ectopic myelinating oligodendrocytes in the dorsal spinal cord as a consequence of altered semaphorin 6D signaling inhibit synapse formation

Jennifer R. Leslie, Fumiyasu Imai, Kaori Fukuhara, Noriko Takegahara, Tilat A. Rizvi, Roland H. Friedel, Fan Wang, Atsushi Kumanogoh, Yutaka Yoshida

Research output: Contribution to journalArticlepeer-review

42 Scopus citations

Abstract

Different types of sensory neurons in the dorsal root ganglia project axons to the spinal cord to convey peripheral information to the central nervous system. Whereas most proprioceptive axons enter the spinal cord medially, cutaneous axons typically do so laterally. Because heavily myelinated proprioceptive axons project to the ventral spinal cord, proprioceptive axons and their associated oligodendrocytes avoid the superficial dorsal horn. However, it remains unclear whether their exclusion from the superficial dorsal horn is an important aspect of neural circuitry. Here we show that a mouse null mutation of Sema6d results in ectopic placement of the shafts of proprioceptive axons and their associated oligodendrocytes in the superficial dorsal horn, disrupting its synaptic organization. Anatomical and electrophysiological analyses show that proper axon positioning does not seem to be required for sensory afferent connectivity with motor neurons. Furthermore, ablation of oligodendrocytes from Sema6d mutants reveals that ectopic oligodendrocytes, but not proprioceptive axons, inhibit synapse formation in Sema6d mutants. Our findings provide new insights into the relationship between oligodendrocytes and synapse formation in vivo, which might be an important element in controlling the development of neural wiring in the central nervous system.

Original languageEnglish
Pages (from-to)4085-4095
Number of pages11
JournalDevelopment (Cambridge)
Volume138
Issue number18
DOIs
StatePublished - 15 Sep 2011

Keywords

  • Mouse
  • Oligodendrocyte
  • Plexin
  • Semaphorin
  • Spinal cord
  • Synapse formation

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