Genetic Fate Mapping Reveals That the Caudal Ganglionic Eminence Produces a Large and Diverse Population of Superficial Cortical Interneurons

By combining an inducible genetic fate mapping strategy with electrophysiological analysis, we have systematically characterized the populations of cortical GABAergic interneurons that originate from the caudal ganglionic eminence (CGE). Interestingly, compared with medial ganglionic eminence (MGE)-derived cortical interneuron populations, the initiation [embryonic day 12.5 (E12.5)] and peak production (E16.5) of interneurons from this embryonic structure occurs 3 d later in development. Moreover, unlike either pyramidal cells or MGE-derived cortical interneurons, CGE-derived interneurons do not integrate into the cortex in an inside-out manner but preferentially (75%) occupy superficial cortical layers independent of birthdate. In contrast to previous estimates, CGE-derived interneurons are both considerably greater in number (∼30% of all cortical interneurons) and diversity (comprised by at least nine distinct subtypes). Furthermore, we found that a large proportion of CGE-derived interneurons, including the neurogliaform subtype, express the glycoprotein Reelin. In fact, most CGE-derived cortical interneurons express either Reelin or vasoactive intestinal polypeptide. Thus, in conjunction with previous studies, we have now determined the spatial and temporal origins of the vast majority of cortical interneuron subtypes.

[1]  O. Marín,et al.  The Embryonic Preoptic Area Is a Novel Source of Cortical GABAergic Interneurons , 2009, The Journal of Neuroscience.

[2]  Maria Blatow,et al.  Two calretinin-positive GABAergic cell types in layer 2/3 of the mouse neocortex provide different forms of inhibition. , 2009, Cerebral cortex.

[3]  H. Tabata,et al.  COUP-TFII Is Preferentially Expressed in the Caudal Ganglionic Eminence and Is Involved in the Caudal Migratory Stream , 2008, The Journal of Neuroscience.

[4]  G. Miyoshi,et al.  The Requirement of Nkx2-1 in the Temporal Specification of Cortical Interneuron Subtypes , 2008, Neuron.

[5]  E. P. Gardner,et al.  Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex , 2008, Nature Reviews Neuroscience.

[6]  B. Cubelos,et al.  Cux‐1 and Cux‐2 control the development of Reelin expressing cortical interneurons , 2008, Developmental neurobiology.

[7]  S. Anderson,et al.  NKX2.1 specifies cortical interneuron fate by activating Lhx6 , 2008, Development.

[8]  M. Delorenzi,et al.  Comprehensive spatiotemporal transcriptomic analyses of the ganglionic eminences demonstrate the uniqueness of its caudal subdivision , 2008, Molecular and Cellular Neuroscience.

[9]  S. Anderson,et al.  A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence. , 2008, Developmental biology.

[10]  S. Anderson,et al.  Fate mapping Nkx2.1‐lineage cells in the mouse telencephalon , 2008, The Journal of comparative neurology.

[11]  G. Fishell,et al.  Mosaic Removal of Hedgehog Signaling in the Adult SVZ Reveals That the Residual Wild-Type Stem Cells Have a Limited Capacity for Self-Renewal , 2007, The Journal of Neuroscience.

[12]  Matthew Grist,et al.  Spatial Genetic Patterning of the Embryonic Neuroepithelium Generates GABAergic Interneuron Diversity in the Adult Cortex , 2007, The Journal of Neuroscience.

[13]  G. Tamás,et al.  Output of Neurogliaform Cells to Various Neuron Types in the Human and Rat Cerebral Cortex , 2007, Frontiers in neural circuits.

[14]  O. Marín,et al.  Delineation of Multiple Subpallial Progenitor Domains by the Combinatorial Expression of Transcriptional Codes , 2007, The Journal of Neuroscience.

[15]  G. Miyoshi,et al.  Physiologically Distinct Temporal Cohorts of Cortical Interneurons Arise from Telencephalic Olig2-Expressing Precursors , 2007, The Journal of Neuroscience.

[16]  P. Arlotta,et al.  Neuronal subtype specification in the cerebral cortex , 2007, Nature Reviews Neuroscience.

[17]  M. Ekker,et al.  Distinct cis-Regulatory Elements from the Dlx1/Dlx2 Locus Mark Different Progenitor Cell Populations in the Ganglionic Eminences and Different Subtypes of Adult Cortical Interneurons , 2007, The Journal of Neuroscience.

[18]  D. Rowitch,et al.  The Proneural Gene Mash1 Specifies an Early Population of Telencephalic Oligodendrocytes , 2007, Journal of Neuroscience.

[19]  A. Sadikot,et al.  Laminar fate of cortical GABAergic interneurons is dependent on both birthdate and phenotype , 2007, The Journal of comparative neurology.

[20]  G. Miyoshi,et al.  Ascl1 defines sequentially generated lineage-restricted neuronal and oligodendrocyte precursor cells in the spinal cord , 2007, Development.

[21]  G. Miyoshi,et al.  Directing neuron-specific transgene expression in the mouse CNS , 2006, Current Opinion in Neurobiology.

[22]  S. Anderson,et al.  The origin and specification of cortical interneurons , 2006, Nature Reviews Neuroscience.

[23]  C. Schuurmans,et al.  A role for proneural genes in the maturation of cortical progenitor cells. , 2006, Cerebral cortex.

[24]  R. Awatramani,et al.  Assembly of the Brainstem Cochlear Nuclear Complex Is Revealed by Intersectional and Subtractive Genetic Fate Maps , 2006, Neuron.

[25]  G. Fishell,et al.  The Temporal and Spatial Origins of Cortical Interneurons Predict Their Physiological Subtype , 2005, Neuron.

[26]  M. Calcagnotto,et al.  Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy , 2005, Nature Neuroscience.

[27]  L. Luo,et al.  Mosaic Analysis with Double Markers in Mice , 2005, Cell.

[28]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[29]  A. Joyner,et al.  Cell Behaviors and Genetic Lineages of the Mesencephalon and Rhombomere 1 , 2004, Neuron.

[30]  H. Tabata,et al.  Birth-date dependent alignment of GABAergic neurons occurs in a different pattern from that of non-GABAergic neurons in the developing mouse visual cortex , 2004, Neuroscience Research.

[31]  Arnold R Kriegstein,et al.  Patterns of neuronal migration in the embryonic cortex , 2004, Trends in Neurosciences.

[32]  S. Anderson,et al.  Origins of Cortical Interneuron Subtypes , 2004, The Journal of Neuroscience.

[33]  L. Tsai,et al.  Control of Cortical Neuron Migration and Layering: Cell and Non Cell-Autonomous Effects of p35 , 2004, The Journal of Neuroscience.

[34]  C. Branda,et al.  Talking about a revolution: The impact of site-specific recombinases on genetic analyses in mice. , 2004, Developmental cell.

[35]  T. Kaneko,et al.  Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67‐GFP knock‐in mouse , 2003, The Journal of comparative neurology.

[36]  O. Marín,et al.  Cell migration in the forebrain. , 2003, Annual review of neuroscience.

[37]  M. Whittington,et al.  A Novel Network of Multipolar Bursting Interneurons Generates Theta Frequency Oscillations in Neocortex , 2003, Neuron.

[38]  G. Tamás,et al.  Identified Sources and Targets of Slow Inhibition in the Neocortex , 2003, Science.

[39]  Kenneth Campbell,et al.  Identification of Two Distinct Progenitor Populations in the Lateral Ganglionic Eminence: Implications for Striatal and Olfactory Bulb Neurogenesis , 2003, The Journal of Neuroscience.

[40]  S. Hestrin,et al.  Synaptic Interactions of Late-Spiking Neocortical Neurons in Layer 1 , 2003, The Journal of Neuroscience.

[41]  G. Fishell,et al.  The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations , 2002, Nature Neuroscience.

[42]  J. Rubenstein,et al.  Modulation of the notch signaling by Mash1 and Dlx1/2 regulates sequential specification and differentiation of progenitor cell types in the subcortical telencephalon. , 2002, Development.

[43]  A. Joyner,et al.  Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. , 2002, Development.

[44]  François Guillemot,et al.  Proneural genes and the specification of neural cell types , 2002, Nature Reviews Neuroscience.

[45]  P. Rakic,et al.  Origin of GABAergic neurons in the human neocortex , 2002, Nature.

[46]  David J. Anderson,et al.  Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. , 2002, Genes & development.

[47]  G. Fishell,et al.  Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain , 2001, Nature Neuroscience.

[48]  B Sakmann,et al.  AMPA Receptor Channels with Long-Lasting Desensitization in Bipolar Interneurons Contribute to Synaptic Depression in a Novel Feedback Circuit in Layer 2/3 of Rat Neocortex , 2001, The Journal of Neuroscience.

[49]  G. Fishell,et al.  In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. , 2001, Development.

[50]  Shankar Srinivas,et al.  Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus , 2001, BMC Developmental Biology.

[51]  Reynaldo Sequerra,et al.  High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP , 2000, Nature Genetics.

[52]  M. Ekker,et al.  A Highly Conserved Enhancer in the Dlx5/Dlx6Intergenic Region is the Site of Cross-Regulatory Interactions betweenDlx Genes in the Embryonic Forebrain , 2000, The Journal of Neuroscience.

[53]  F. Guillemot,et al.  A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. , 2000, Genes & development.

[54]  J. Richardson,et al.  Correct Coordination of Neuronal Differentiation Events in Ventral Forebrain Requires the bHLH Factor MASH1 , 1999, Molecular and Cellular Neuroscience.

[55]  O. Marín,et al.  Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. , 1999, Development.

[56]  A. Guidotti,et al.  Cortical bitufted, horizontal, and Martinotti cells preferentially express and secrete reelin into perineuronal nets, nonsynaptically modulating gene expression. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[57]  F. Guillemot,et al.  Mash1 regulates neurogenesis in the ventral telencephalon. , 1999, Development.

[58]  Philippe Soriano.  Generalized lacZ expression with the ROSA26 Cre reporter strain , 1999, Nature Genetics.

[59]  C. Sotelo,et al.  Regional and Cellular Patterns of reelin mRNA Expression in the Forebrain of the Developing and Adult Mouse , 1998, The Journal of Neuroscience.

[60]  A. Fairén,et al.  Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex , 1998, The Journal of comparative neurology.

[61]  A. Guidotti,et al.  Reelin is preferentially expressed in neurons synthesizing gamma-aminobutyric acid in cortex and hippocampus of adult rats. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Leyuan Shi,et al.  Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. , 1997, Science.

[63]  I. Kill.  Localisation of the Ki-67 antigen within the nucleolus. Evidence for a fibrillarin-deficient region of the dense fibrillar component. , 1996, Journal of cell science.

[64]  Y. Kubota,et al.  Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  M. Seike,et al.  The reeler gene-associated antigen on cajal-retzius neurons is a crucial molecule for laminar organization of cortical neurons , 1995, Neuron.

[66]  Y. Kawaguchi.  Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  J. D. del Río,et al.  Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody. , 1995, Cerebral cortex.

[68]  Y. Kubota,et al.  Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex , 1994, Brain Research.

[69]  A. Joyner,et al.  Dynamic expression of the murine Achaete-Scute homologue Mash-1 in the developing nervous system , 1993, Mechanisms of Development.

[70]  J. Rogers.  Immunohistochemical markers in rat cortex: co-localization of calretinin and calbindin-D28k with neuropeptides and GABA , 1992, Brain Research.

[71]  Yamamura Ken-ichi,et al.  Efficient selection for high-expression transfectants with a novel eukaryotic vector , 1991 .

[72]  H. Niwa,et al.  Efficient selection for high-expression transfectants with a novel eukaryotic vector. , 1991, Gene.

[73]  P. Derer,et al.  Cajal-retzius cell ontogenesis and death in mouse brain visualized with horseradish peroxidase and electron microscopy , 1990, Neuroscience.

[74]  David J. Anderson,et al.  Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors , 1990, Nature.

[75]  J. Parnavelas,et al.  Development of vasoactive‐intestinal‐polypeptide‐immunoreactive neurons in the rat occipital cortex: A combined immunohistochemical‐autoradiographic study , 1989, The Journal of comparative neurology.

[76]  A. Fairén,et al.  Times of generation of glutamic acid decarboxylase immunoreactive neurons in mouse somatosensory cortex , 1986, The Journal of comparative neurology.

[77]  M. Miller,et al.  Cogeneration of retrogradely labeled corticocortical projection and GABA-immunoreactive local circuit neurons in cerebral cortex. , 1985, Brain research.

[78]  P. Emson,et al.  Development of vasoactive intestinal polypeptide (VIP) containing neurones in the rat brain , 1979, Brain Research.

[79]  R. Sidman,et al.  Autoradiographic Study of Cell Migration during Histogenesis of Cerebral Cortex in the Mouse , 1961, Nature.

[80]  J. Hirschfeld,et al.  Distribution of Group-specific Components (Gc) in the Sera of Native Africans , 1961, Nature.

[81]  S. Anderson,et al.  NKX 2 . 1 specifies cortical interneuron fate by activating Lhx 6 , 2022 .