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1 The Rockefeller University, New York, NY 10021, USA
2 The Skirball Institute of Biomolecular Medicine, New York University School of Medicine, New York, NY 10016, USA
3 University of California, San Francisco, Department of Neurosurgery and Anatomy, San Francisco, CA 94143, USA
* Present address: Hynek Wichterle, Howard Hughes Medical Institute, Center for Neurobiology and Behavior, Columbia University, 1013 Hammer Health Sciences Center, 701 West 168th St, New York, NY 10032, USA
Author for correspondence (e-mail: abuylla{at}itsa.ucsf.edu)
Accepted July 2, 2001
Recent studies suggest that neurons born in the developing basal forebrain migrate long distances perpendicularly to radial glia and that many of these cells reach the developing neocortex. This form of tangential migration, however, has not been demonstrated in vivo, and the sites of origin, pathways of migration and final destinations of these neurons in the postnatal brain are not fully understood. Using ultrasound-guided transplantation in utero, we have mapped the migratory pathways and fates of cells born in the lateral and medial ganglionic eminences (LGE and MGE) in 13.5-day-old mouse embryos. We demonstrate that LGE and MGE cells migrate along different routes to populate distinct regions in the developing brain. We show that LGE cells migrate ventrally and anteriorly, and give rise to the projecting medium spiny neurons in the striatum, nucleus accumbens and olfactory tubercle, and to granule and periglomerular cells in the olfactory bulb. By contrast, we show that the MGE is a major source of neurons migrating dorsally and invading the developing neocortex. MGE cells migrate into the neocortex via the neocortical subventricular zone and differentiate into the transient subpial granule neurons in the marginal zone and into a stable population of GABA-, parvalbumin- or somatostatin-expressing interneurons throughout the cortical plate.
Key words: Ganglionic eminences, Neocortical development, Tangential neuronal migration, Ultrasound, Fate map, Non-pyramidal, Interneurons, Medium spiny neurons, GABA, Parvalbumin, Somatostatin, DARPP-32, Mouse
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J. A. Siegenthaler and M. W. Miller Transforming Growth Factor {beta}1 Modulates Cell Migration in Rat Cortex: Effects of Ethanol Cereb Cortex, July 1, 2004; 14(7): 791 - 802. [Abstract] [Full Text] [PDF]
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J. E. Crandall, H. E. Hackett, S. A. Tobet, B. E. Kosofsky, and P. G. Bhide Cocaine Exposure Decreases GABA Neuron Migration from the Ganglionic Eminence to the Cerebral Cortex in Embryonic Mice Cereb Cortex, June 1, 2004; 14(6): 665 - 675. [Abstract] [Full Text] [PDF]
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F. Moya and M. Valdeolmillos Polarized Increase of Calcium and Nucleokinesis in Tangentially Migrating Neurons Cereb Cortex, June 1, 2004; 14(6): 610 - 618. [Abstract] [Full Text] [PDF]
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Q. Xu, I. Cobos, E. De La Cruz, J. L. Rubenstein, and S. A. Anderson Origins of Cortical Interneuron Subtypes J. Neurosci., March 17, 2004; 24(11): 2612 - 2622. [Abstract] [Full Text] [PDF]
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T. Nomura and N. Osumi Misrouting of mitral cell progenitors in the Pax6/small eyerat telencephalon Development, February 15, 2004; 131(4): 787 - 796. [Abstract] [Full Text] [PDF]
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V. Hammond, L.-H. Tsai, and S.-S. Tan Control of Cortical Neuron Migration and Layering: Cell and Non Cell-Autonomous Effects of p35 J. Neurosci., January 14, 2004; 24(2): 576 - 587. [Abstract] [Full Text] [PDF]
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D. Tanaka, Y. Nakaya, Y. Yanagawa, K. Obata, and F. Murakami Multimodal tangential migration of neocortical GABAergic neurons independent of GPI-anchored proteins Development, December 1, 2003; 130(23): 5803 - 5813. [Abstract] [Full Text] [PDF]
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J. M. Stenman, B. Wang, and K. Campbell Tlx Controls Proliferation and Patterning of Lateral Telencephalic Progenitor Domains J. Neurosci., November 19, 2003; 23(33): 10568 - 10576. [Abstract] [Full Text] [PDF]
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J. G. Corbin, M. Rutlin, N. Gaiano, and G. Fishell Combinatorial function of the homeodomain proteins Nkx2.1 and Gsh2 in ventral telencephalic patterning Development, October 15, 2003; 130(20): 4895 - 4906. [Abstract] [Full Text] [PDF]
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J. Morante-Oria, A. Carleton, B. Ortino, E. J. Kremer, A. Fairen, and P.-M. Lledo Subpallial origin of a population of projecting pioneer neurons during corticogenesis PNAS, October 14, 2003; 100(21): 12468 - 12473. [Abstract] [Full Text] [PDF]
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S. Rakic and N. Zecevic Emerging Complexity of Layer I in Human Cerebral Cortex Cereb Cortex, October 1, 2003; 13(10): 1072 - 1083. [Abstract] [Full Text] [PDF]
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S. Nery, J. G. Corbin, and G. Fishell Dlx2 Progenitor Migration in Wild Type and Nkx2.1 Mutant Telencephalon Cereb Cortex, September 1, 2003; 13(9): 895 - 903. [Abstract] [Full Text] [PDF]
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P. W. Land and A. P. Monaghan Expression of the Transcription Factor, tailless, Is Required for Formation of Superficial Cortical Layers Cereb Cortex, September 1, 2003; 13(9): 921 - 931. [Abstract] [Full Text] [PDF]
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G. Liu and Y. Rao Neuronal Migration from the Forebrain to the Olfactory Bulb Requires a New Attractant Persistent in the Olfactory Bulb J. Neurosci., July 23, 2003; 23(16): 6651 - 6659. [Abstract] [Full Text] [PDF]
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E. S. B. C. Ang Jr, T. F. Haydar, V. Gluncic, and P. Rakic Four-Dimensional Migratory Coordinates of GABAergic Interneurons in the Developing Mouse Cortex J. Neurosci., July 2, 2003; 23(13): 5805 - 5815. [Abstract] [Full Text] [PDF]
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H. Valcanis and S.-S. Tan Layer Specification of Transplanted Interneurons in Developing Mouse Neocortex J. Neurosci., June 15, 2003; 23(12): 5113 - 5122. [Abstract] [Full Text] [PDF]
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