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Articles, Development/Plasticity/Repair

Hippocampal Pyramidal Neurons Switch from a Multipolar Migration Mode to a Novel “Climbing” Migration Mode during Development

Ayako Kitazawa, Ken-ichiro Kubo, Kanehiro Hayashi, Yuki Matsunaga, Kazuhiro Ishii and Kazunori Nakajima
Journal of Neuroscience 22 January 2014, 34 (4) 1115-1126; DOI: https://doi.org/10.1523/JNEUROSCI.2254-13.2014
Ayako Kitazawa
Department of Anatomy, Keio University School of Medicine, Shinjuku-ku, Tokyo, 160-8582, Japan
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Ken-ichiro Kubo
Department of Anatomy, Keio University School of Medicine, Shinjuku-ku, Tokyo, 160-8582, Japan
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Kanehiro Hayashi
Department of Anatomy, Keio University School of Medicine, Shinjuku-ku, Tokyo, 160-8582, Japan
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Yuki Matsunaga
Department of Anatomy, Keio University School of Medicine, Shinjuku-ku, Tokyo, 160-8582, Japan
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Kazuhiro Ishii
Department of Anatomy, Keio University School of Medicine, Shinjuku-ku, Tokyo, 160-8582, Japan
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Kazunori Nakajima
Department of Anatomy, Keio University School of Medicine, Shinjuku-ku, Tokyo, 160-8582, Japan
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Abstract

The hippocampus plays important roles in brain functions. Despite the importance of hippocampal functions, recent analyses of neuronal migration have mainly been performed on the cerebral neocortex, and the cellular mechanisms responsible for the formation of the hippocampus are not yet completely understood. Moreover, why a prolonged time is required for hippocampal neurons to complete their migration has been unexplainable for several decades. We analyzed the migratory profile of neurons in the developing mouse hippocampal CA1 region and found that the hippocampal pyramidal neurons generated near the ventricle became postmitotic multipolar cells and accumulated in the multipolar cell accumulation zone (MAZ) in the late stage of development. The hippocampal neurons passed through the pyramidal layer by a unique mode of migration. Their leading processes were highly branched and made contact with many radial fibers. Time-lapse imaging revealed that the migrating cells changed their scaffolds from the original radial fibers to other radial fibers, and as a result they proceed in a zigzag manner, with long intervals. The migrating cells in the hippocampus reminded us of “rock climbers” that instead of using their hands to pull up their bodies were using their leading processes to pull up their cell bodies. Because this mode of migration had never been described, we called it the “climbing” mode. The change from the “climbing” mode in the hippocampus to the “locomotion” mode in the neocortex may have contributed to the brain expansion during evolution.

  • cortex
  • development
  • hippocampus
  • migration
  • neuron
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The Journal of Neuroscience: 34 (4)
Journal of Neuroscience
Vol. 34, Issue 4
22 Jan 2014
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Hippocampal Pyramidal Neurons Switch from a Multipolar Migration Mode to a Novel “Climbing” Migration Mode during Development
Ayako Kitazawa, Ken-ichiro Kubo, Kanehiro Hayashi, Yuki Matsunaga, Kazuhiro Ishii, Kazunori Nakajima
Journal of Neuroscience 22 January 2014, 34 (4) 1115-1126; DOI: 10.1523/JNEUROSCI.2254-13.2014

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Hippocampal Pyramidal Neurons Switch from a Multipolar Migration Mode to a Novel “Climbing” Migration Mode during Development
Ayako Kitazawa, Ken-ichiro Kubo, Kanehiro Hayashi, Yuki Matsunaga, Kazuhiro Ishii, Kazunori Nakajima
Journal of Neuroscience 22 January 2014, 34 (4) 1115-1126; DOI: 10.1523/JNEUROSCI.2254-13.2014
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Keywords

  • cortex
  • development
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  • migration
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