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The Journal of Neuroscience, May 10, 2006, 26(19):5017-5027; doi:10.1523/JNEUROSCI.0272-06.2006

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Development/Plasticity/Repair
Translocation of Synaptically Connected Interneurons across the Dentate Gyrus of the Early Postnatal Rat Hippocampus

Yury M. Morozov, Albert E. Ayoub, and Pasko Rakic

Department of Neurobiology and Kavli Institute for Neuroscience, Yale University School of Medicine, New Haven, Connecticut 06510

Correspondence should be addressed to Dr. Pasko Rakic, Department of Neurobiology, Yale University School of Medicine, P.O. Box 208001, New Haven, CT 06510-8001. Email: pasko.rakic{at}yale.edu

Most neurons in the developing mammalian brain migrate to their final destinations by translocation of the cell nucleus within their leading process and immature bipolar body that is devoid of synaptic connections. Here, we used a combination of immunohistochemistry at light- and electron-microscopic (EM) levels and time-lapse imaging in slice cultures to analyze migration of synaptically interconnected, cholecystokinin-immunopositive [CCK(+)] interneurons in the dentate gyrus in the rat hippocampus during early postnatal ages. We observed dynamic morphogenetic transformation of the CCK(+) interneurons, from a horizontal bipolar shape situated in the molecular layer, through a transitional triangular and then vertical bipolar form that they acquire while traversing the granular layer to finally assume an adult-like pyramidal-shaped morphology on entering the hilus. Immunostaining with anti-glial fibrillary acidic protein and three-dimensional reconstructions from serial EM images indicate that, unlike granule cells, which migrate from the hilus to the granular layer, interneurons traverse this layer in the opposite direction without apparent surface-mediated guidance of the radial glial cells. Importantly, the somas, dendrites, and axons of the CCK(+) transitional forms maintain old and acquire new synaptic contacts while migrating across the dentate plate. The migration of synaptically interconnected neurons that may occur in response to local functional demand represents a novel mode of cell movement and form of neuroplasticity.

Key words: cholecystokinin; development; migration; innervation; electron microscopy; 3D reconstruction; live imaging

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Received Jan. 20, 2006; revised March 7, 2006; accepted April 1, 2006.

Correspondence should be addressed to Dr. Pasko Rakic, Department of Neurobiology, Yale University School of Medicine, P.O. Box 208001, New Haven, CT 06510-8001. Email: pasko.rakic{at}yale.edu

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