In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain
Abstract
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.
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The MGE and adjacent POA generate virtually all SST+ and PV+ cortical interneurons.
“The MGE and adjacent POA generate virtually all interneurons in the SST+ and PV+ classes”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Wichterle et al., 2001
Interneurons spread through the developing cortex by two main streams, a superficial marginal zone route and a deep subventricular zone route, with a smaller subplate route.
“Interneurons disperse throughout the developing cortex via two large migratory streams, a superficial route that courses through the marginal zone (MZ), and a deep route that largely overlaps with the pallial subventricular zone (SVZ) (Lavdas et al., 1999; Wichterle et al., 2001). A smaller fraction of interneurons migrates through the subplate.”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Wichterle et al., 2001
More than 80% of Dlx6a-Cre fate mapped cortical cells at E18.5 mapped to precursor state 1 based on expression of canonical regulators of interneuron development.
“we found that, as expected20, more than 80% of Dlx6a-Cre fate mapped cortical cells at E18.5 mapped to precursor state 1, based on their expression of canonical regulators of interneuron development”
From Developmental diversification of cortical inhibitory interneurons (2018) · cites this paper as [20]
MGE- and CGE-derived interneurons reach the dorsal telencephalon via separate pathways: MGE-derived cells travel via dorsolateral routes, while CGE-derived cells follow three distinct routes laterally, medially, and caudally.
“MGE- and CGE-derived interneurons reach the dorsal telencephalon via separate pathways: those from the MGE travel via dorsolateral routes while those from the CGE follow three distinct routes laterally, medially, and caudally.”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1202]
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- Authors
- Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G., & Alvarez-Buylla, A.
- Affiliations
- Howard Hughes Medical Institute (US)
- The Rockefeller University, New York, NY 10021, USA
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2001-10-01
- Volume
- 128
- Issue
- 19
- Pages
- 3759-3771
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2159617943
- Cited by
- 722
- References
- 68
- Citations by year
- 2026: 10 · 2025: 18 · 2024: 15 · 2023: 15 · 2022: 11 · 2021: 23 · 2020: 27 · 2019: 19 · 2018: 25 · 2017: 23 · 2016: 25 · 2015: 20 · 2014: 29 · 2013: 41 · 2012: 32
- FWCI
- 7.93
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Development (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (NS 39007, NS 38461, R01NS038461, R01NS039007)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD32116)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- tangential migration, basal forebrain, lateral ganglionic eminence, medial ganglionic eminence, neocortex, olfactory bulb, striatum, nucleus accumbens, olfactory tubercle, interneurons, subventricular zone, parvalbumin, somatostatin, GABAergic neurons, mouse embryo
- MeSH terms
- Animals, Cell Differentiation, Cell Movement, Cerebral Cortex, Embryonic Induction, Female, gamma-Aminobutyric Acid, Ganglia, Humans, Mice, Inbred Strains, Mice, Transgenic, Nerve Tissue Proteins, Neuroglia, Neurons, Olfactory Bulb, Parvalbumins, Phosphoproteins, Somatostatin, Telencephalon, Ultrasonography, Prenatal, Prosencephalon, Cell Transplantation, Mice, Dopamine and cAMP-Regulated Phosphoprotein 32
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