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Research Article

Axon position within the corpus callosum determines contralateral cortical projection

Jing Zhou, Yunqing Wen, Liang She, Ya-nan Sui, Lu Liu, Linda J. Richards, and Mu-ming Poo
PNAS July 16, 2013 110 (29) E2714-E2723; https://doi.org/10.1073/pnas.1310233110
Jing Zhou
aInstitute of Neuroscience, State Key Laboratory of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
bUniversity of Chinese Academy of Sciences, Shanghai 200031, China;
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Yunqing Wen
aInstitute of Neuroscience, State Key Laboratory of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
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Liang She
aInstitute of Neuroscience, State Key Laboratory of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
bUniversity of Chinese Academy of Sciences, Shanghai 200031, China;
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Ya-nan Sui
aInstitute of Neuroscience, State Key Laboratory of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
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Lu Liu
aInstitute of Neuroscience, State Key Laboratory of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
bUniversity of Chinese Academy of Sciences, Shanghai 200031, China;
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Linda J. Richards
cQueensland Brain Institute and
dSchool of Biomedical Sciences, the University of Queensland, Brisbane, Queensland, 4072, Australia; and
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Mu-ming Poo
aInstitute of Neuroscience, State Key Laboratory of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
eDepartment of Molecular and Cell Biology, Helen Wills Neuroscience Institute, University of California, Berkeley, CA 94720
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  • For correspondence: mpoo@berkeley.edu
  1. Contributed by Mu-ming Poo, May 30, 2013 (sent for review May 1, 2013)

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Significance

Two hemispheres of the neocortex are connected via a large axon bundle, the corpus callosum (CC). Axons from one side of the cortex project primarily to the equivalent cortical area on the contralateral side. How this homotopic axon projection is achieved during development remains unclear. Quantitative analysis of the cortical axons' positions within CC and their projection pattern after crossing the midline showed that axon position within CC is critical for homotopic projection. Further genetic perturbations of semaphorin/neuropilin-1 signaling disrupted the axon order in CC, resulting in an ectopic contralateral axon projection that could not be corrected by developmental refinement.

Abstract

How developing axons in the corpus callosum (CC) achieve their homotopic projection to the contralateral cortex remains unclear. We found that axonal position within the CC plays a critical role in this projection. Labeling of nearby callosal axons in mice showed that callosal axons were segregated in an orderly fashion, with those from more medial cerebral cortex located more dorsally and subsequently projecting to more medial contralateral cortical regions. The normal axonal order within the CC was grossly disturbed when semaphorin3A/neuropilin-1 signaling was disrupted. However, the order in which axons were positioned within the CC still determined their contralateral projection, causing a severe disruption of the homotopic contralateral projection that persisted at postnatal day 30, when the normal developmental refinement of contralateral projections is completed in wild-type (WT) mice. Thus, the orderly positioning of axons within the CC is a primary determinant of how homotopic interhemispheric projections form in the contralateral cortex.

  • axon development
  • axon fiber order
  • cortical axon guidance
  • cortical development

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: mpoo{at}berkeley.edu.
  • Author contributions: J.Z., L.J.R., and M.-m.P. designed research; J.Z. performed research; J.Z., Y.W., L.S., Y.-n.S., and L.L. analyzed data; and J.Z., L.J.R., and M.-m.P. wrote the paper.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1310233110/-/DCSupplemental.

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Axon order determines the callosal projection
Jing Zhou, Yunqing Wen, Liang She, Ya-nan Sui, Lu Liu, Linda J. Richards, Mu-ming Poo
Proceedings of the National Academy of Sciences Jul 2013, 110 (29) E2714-E2723; DOI: 10.1073/pnas.1310233110

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Axon order determines the callosal projection
Jing Zhou, Yunqing Wen, Liang She, Ya-nan Sui, Lu Liu, Linda J. Richards, Mu-ming Poo
Proceedings of the National Academy of Sciences Jul 2013, 110 (29) E2714-E2723; DOI: 10.1073/pnas.1310233110
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