Radial and tangential migration of telencephalic somatostatin neurons originated from the mouse diagonal area

The telencephalic subpallium is the source of various GABAergic interneuron cohorts that invade the pallium via tangential migration. Based on genoarchitectonic studies, the subpallium has been subdivided into four major domains: striatum, pallidum, diagonal area and preoptic area (Puelles et al. 2013; Allen Developing Mouse Brain Atlas), and a larger set of molecularly distinct progenitor areas (Flames et al. 2007). Fate mapping, genetic lineage-tracing studies, and other approaches have suggested that each subpallial subdivision produces specific sorts of inhibitory interneurons, distinguished by differential peptidic content, which are distributed tangentially to pallial and subpallial target territories (e.g., olfactory bulb, isocortex, hippocampus, pallial and subpallial amygdala, striatum, pallidum, septum). In this report, we map descriptively the early differentiation and apparent migratory dispersion of mouse subpallial somatostatin-expressing (Sst) cells from E10.5 onward, comparing their topography with the expression patterns of the genes Dlx5, Gbx2, Lhx7-8, Nkx2.1, Nkx5.1 (Hmx3), and Shh, which variously label parts of the subpallium. Whereas some experimental results suggest that Sst cells are pallidal, our data reveal that many, if not most, telencephalic Sst cells derive from de diagonal area (Dg). Sst-positive cells initially only present at the embryonic Dg selectively populate radially the medial part of the bed nucleus striae terminalis (from paraseptal to amygdaloid regions) and part of the central amygdala; they also invade tangentially the striatum, while eschewing the globus pallidum and the preoptic area, and integrate within most cortical and nuclear pallial areas between E10.5 and E16.5.

• Publication year

  2015

• Venue

  Brain Structure and Function

• Publication date

  2015-07-19

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1007/s00429-015-1086-8PMID 26189100PMCID 4920861
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• A Comparative Perspective on Wnt/β-Catenin Signalling in Cell Fate Determination.

  2017cited by this paper
• Fgf signaling controls the telencephalic distribution of Fgf-expressing progenitors generated in the rostral patterning center

  2015cited by this paper
• Exploring Brain Genoarchitecture by Single and Double Chromogenic In Situ Hybridization (ISH) and Immunohistochemistry (IHC) on Cryostat, Paraffin, or Floating Sections

  2015cited by this paper
• Exploring Brain Genoarchitecture by Single and Double Chromogenic In Situ Hybridization (ISH) and Immunohistochemistry (IHC) in Whole-Mount Embryos

  2015cited by this paper
• Gene Maps and Related Histogenetic Domains in the Forebrain and Midbrain

  2015cited by this paper
• Development and Evolution of the Claustrum

  2014influential reference
• The claustrum : structural, functional, and clinical neuroscience

  2014influential reference
• Subcortical origins of human and monkey neocortical interneurons

  2013cited by this paper
• Cellular and molecular mechanisms controlling the migration of neocortical interneurons

  2013cited by this paper
• A developmental ontology for the mammalian brain based on the prosomeric model.

  2013influential reference
• The Basal Forebrain Cholinergic Projection System in Mice Neuron Types in the Basal Forebrain - Chapter 28 The Mouse Nervous System

  2012cited by this paper
• Chapter 7 – Subpallial Structures

  2012influential reference
• The Mouse Nervous System.

  2012influential reference
• Chapter 8 – Hypothalamus

  2012influential reference
• Jasper's basic mechanisms of the epilepsies

  2012cited by this paper
• Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala

  2011influential reference
• Pallial origin of basal forebrain cholinergic neurons in the nucleus basalis of Meynert and horizontal limb of the diagonal band nucleus

  2011cited by this paper
• Lhx6 and Lhx8 coordinately induce neuronal expression of Shh that controls the generation of interneuron progenitors.

  2011cited by this paper
• Genetic and experimental evidence supports the continuum of the central extended amygdala and a mutiple embryonic origin of its principal neurons

  2011cited by this paper
• A Wide Diversity of Cortical GABAergic Interneurons Derives from the Embryonic Preoptic Area

  2011influential reference
• Sonic hedgehog signaling confers ventral telencephalic progenitors with distinct cortical interneuron fates.

  2010cited by this paper
• Sonic hedgehog expressing and responding cells generate neuronal diversity in the medial amygdala

  2010influential reference
• The Progenitor Zone of the Ventral Medial Ganglionic Eminence Requires Nkx2-1 to Generate Most of the Globus Pallidus But Few Neocortical Interneurons

  2010influential reference
• Topography of Somatostatin Gene Expression Relative to Molecular Progenitor Domains during Ontogeny of the Mouse Hypothalamus

  2010cited by this paper
• Generation of interneuron diversity in the mouse cerebral cortex

  2010cited by this paper
• The Mouse Homeobox Gene Gbx2 Is Required for the Development of Cholinergic Interneurons in the Striatum

  2010cited by this paper
• Genetic Fate Mapping Reveals That the Caudal Ganglionic Eminence Produces a Large and Diverse Population of Superficial Cortical Interneurons

  2010cited by this paper
• Dlx5 and Dlx6 Regulate the Development of Parvalbumin-Expressing Cortical Interneurons

  2010cited by this paper
• Ontogenetic Expression of Sonic Hedgehog in the Chicken Subpallium

  2010cited by this paper
• The Largest Group of Superficial Neocortical GABAergic Interneurons Expresses Ionotropic Serotonin Receptors

  2010cited by this paper
• A genomic atlas of mouse hypothalamic development

  2010cited by this paper
• A neuronal migratory pathway crossing from diencephalon to telencephalon populates amygdala nuclei

  2010cited by this paper
• Somatostatin and somatostatin receptors.

  2010cited by this paper
• Cellular peptide hormone synthesis and secretory pathways

  2010cited by this paper
• The generation of cortical interneurons

  2010cited by this paper
• Cerebral Cortex doi:10.1093/cercor/bhp038 Characterization of Nkx6-2-Derived

  2009influential reference
• The Embryonic Preoptic Area Is a Novel Source of Cortical GABAergic Interneurons

  2009influential reference
• Expression of somatostatin and neuropeptide Y in the embryonic, postnatal, and adult mouse amygdalar complex

  2009influential reference
• Chemoarchitectonic Atlas of the Mouse Brain

  2009cited by this paper
• The Somatostatin 2A Receptor Is Enriched in Migrating Neurons during Rat and Human Brain Development and Stimulates Migration and Axonal Outgrowth

  2009cited by this paper
• Somatostatinergic systems in brain: networks and functions.

  2008cited by this paper
• Fate mapping Nkx2.1‐lineage cells in the mouse telencephalon

  2008influential reference
• Histogenetic compartments of the mouse centromedial and extended amygdala based on gene expression patterns during development

  2008cited by this paper
• A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence.

  2008influential reference
• The LIM-Homeobox Gene Islet-1 Is Required for the Development of Restricted Forebrain Cholinergic Neurons

  2008cited by this paper
• Spatial Genetic Patterning of the Embryonic Neuroepithelium Generates GABAergic Interneuron Diversity in the Adult Cortex

  2007influential reference
• Lhx6 Activity Is Required for the Normal Migration and Specification of Cortical Interneuron Subtypes

  2007influential reference
• Delineation of Multiple Subpallial Progenitor Domains by the Combinatorial Expression of Transcriptional Codes

  2007influential reference
• 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

  2007cited by this paper
• The origin and specification of cortical interneurons

  2006cited by this paper
• Chicken lateral septal organ and other circumventricular organs form in a striatal subdomain abutting the molecular striatopallidal border

  2006cited by this paper
• The temporal and spatial origins of cortical interneurons predict their physiological subtype.

  2005influential reference
• Development of neurons and fibers containing calcium binding proteins in the pallial amygdala of mouse, with special emphasis on those of the basolateral amygdalar complex

  2005cited by this paper
• CHAPTER 1 – Gene Maps and Related Histogenetic Domains in the Forebrain and Midbrain

  2004cited by this paper
• Expression of Dbx1, Neurogenin 2, Semaphorin 5A, Cadherin 8, and Emx1 distinguish ventral and lateral pallial histogenetic divisions in the developing mouse claustroamygdaloid complex

  2004influential reference
• LIM Genes Parcellate the Embryonic Amygdala and Regulate Its Development

  2004cited by this paper
• Origins of Cortical Interneuron Subtypes

  2004influential reference
• CHAPTER 19 – Amygdala and Extended Amygdala of the Rat: A Cytoarchitectonical, Fibroarchitectonical, and Chemoarchitectonical Survey

  2004cited by this paper
• Dlx2 progenitor migration in wild type and Nkx2.1 mutant telencephalon.

  2003cited by this paper
• The mouse brain in stereotaxic coordinates

  2003cited by this paper
• Identification of Two Distinct Progenitor Populations in the Lateral Ganglionic Eminence: Implications for Striatal and Olfactory Bulb Neurogenesis

  2003cited by this paper
• Cell migration in the forebrain.

  2003cited by this paper
• Early differences in axonal outgrowth, cell migration and GABAergic differentiation properties between the dorsal and lateral cortex.

  2003cited by this paper
• The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain

  2003influential reference
• The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations

  2002cited by this paper
• Cortical Excitatory Neurons and Glia, But Not GABAergic Neurons, Are Produced in the Emx1-Expressing Lineage

  2002cited by this paper
• in the figures anterior commissure basal ganglia neuroepithelium of the basal ganglia basal telencephalon dorsolateral intercalated mass of the amygdala presumptive intercalated mass of the amygdala intermediate zone

  2002cited by this paper
• Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons.

  2002cited by this paper
• Origin of GABAergic neurons in the human neocortex

  2002cited by this paper
• Stage-specific control of neuronal migration by somatostatin

  2002cited by this paper
• Distinct cortical migrations from the medial and lateral ganglionic eminences.

  2001cited by this paper
• Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain

  2001cited by this paper
• A long, remarkable journey: Tangential migration in the telencephalon

  2001cited by this paper
• Multipotent Stem Cells from the Mouse Basal Forebrain Contribute GABAergic Neurons and Oligodendrocytes to the Cerebral Cortex during Embryogenesis

  2001cited by this paper
• Translating developmental time across mammalian species.

  2001influential reference
• Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex

  2000cited by this paper
• The murine Otp homeobox gene plays an essential role in the specification of neuronal cell lineages in the developing hypothalamus.

  2000cited by this paper
• Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx‐2, Emx‐1, Nkx‐2.1, Pax‐6, and Tbr‐1

  2000influential reference
• Hmx: an evolutionary conserved homeobox gene family expressed in the developing nervous system in mice and Drosophila.

  2000cited by this paper
• The amygdala.

  2000cited by this paper
• DLX‐1, DLX‐2, and DLX‐5 expression define distinct stages of basal forebrain differentiation

  1999cited by this paper
• 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.

  1999influential reference
• What is the amygdala?

  1998cited by this paper
• The Specification of Neuronal Fate: A Common Precursor for Neurotransmitter Subtypes in the Rat Cerebral Cortex In Vitro

  1995cited by this paper
• T-brain-1: a homolog of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex.

  1995cited by this paper
• Longitudinal organization of the anterior neural plate and neural tube.

  1995cited by this paper
• The neurobiology of somatostatin.

  1994cited by this paper
• Development and early postnatal maturation of the primary olfactory cortex.

  1994cited by this paper
• The embryonic vertebrate forebrain: the prosomeric model.

  1994cited by this paper
• Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt- 3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries

  1993influential reference
• Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization.

  1993cited by this paper
• Peptide immunoreactive neurons in the amygdala and the bed nucleus of the stria terminalis project to the midbrain central gray in the rat.

  1992cited by this paper
• Ontogeny of transmitters and peptides in the CNS

  1992cited by this paper
• Differential distribution of immunohistochemical markers in the bed nucleus of the stria terminalis in the human brain.

  1991cited by this paper
• The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain.

  1991cited by this paper
• The House Mouse

  1989cited by this paper
• Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat: I. cytoarchitecture

  1989cited by this paper
• Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat: II. chemoarchitecture

  1989cited by this paper
• Neurogenetic and morphogenetic heterogeneity in the bed nucleus of the stria terminalis

  1987cited by this paper
• Evidence for corticotropin‐releasing factor, neurotensin, and somatostatin in the neural pathway from the central nucleus of the amygdala to the parabrachial nucleus

  1985cited by this paper

• Selective Lis1 inactivation disrupts migration and positioning of cortical somatostatin interneurons

  2026cites this paper
• Transcriptomics reveals pallial and subpallial subdivisions of the mouse medial amygdala

  2026cites this paper
• Cortical Type: The Basis for a Modern Neurodevelopmental Synthesis (Ontogeny, Phylogeny, Synaptic Connectivity) of the Human Cerebral Cortex

  2026cites this paper
• Elucidating the neuromeric organization of the Mongolian gerbil brain

  2025cites this paper
• Multi-neuromeric origin of tyrosine hydroxylase-positive neurons within the substantia nigra and ventral tegmental area

  2025cites this paper
• Developmental mouse brain common coordinate framework

  2024cites this paper
• Ramón y Cajal’s ‘lenticular tract’ represents infrasubthalamic pyramidal collaterals targeting mesodiencephalic centers: an obscure misunderstood aspect of the motor pathway clarified by Allen Mouse Brain Connectivity data

  2024cites this paper
• Development and function of the medial amygdala.

  2024cites this paper
• An illustrated summary of the prosomeric model

  2024influential citation
• Expansion modes of primate nervous system structures in the light of the Prosomeric Model

  2023cites this paper
• Critical test of the assumption that the hypothalamic entopeduncular nucleus of rodents is homologous with the primate internal pallidum

  2023influential citation
• Prosomeric Hypothalamic Distribution of Tyrosine Hydroxylase Positive Cells in Adolescent Rats

  2022cites this paper
• Cytology, architecture, development, and connections of the primate striatum: Hints for human pathology.

  2022cites this paper
• GABAergic neurons maturation is regulated by a delicate network

  2022cites this paper
• Evolution and Development of Amygdala Subdivisions: Pallial, Subpallial, and Beyond

  2022cites this paper
• Editorial: In the footsteps of the prosomeric model

  2022cites this paper
• Developmental-Based Classification of Enkephalin and Somatostatin Containing Neurons of the Chicken Central Extended Amygdala

  2022cites this paper
• Single cell enhancer activity distinguishes GABAergic and cholinergic lineages in embryonic mouse basal ganglia

  2022cites this paper
• Tangential Intrahypothalamic Migration of the Mouse Ventral Premamillary Nucleus and Fgf8 Signaling

  2021cites this paper
• A novel telencephalon‐opto‐hypothalamic morphogenetic domain coexpressing Foxg1 and Otp produces most of the glutamatergic neurons of the medial extended amygdala

  2021cites this paper
• Salient brain entities labelled in P2rx7-EGFP reporter mouse embryos include the septum, roof plate glial specializations and circumventricular ependymal organs

  2021cites this paper
• Single Cell Enhancer Activity Maps Neuronal Lineages in Embryonic Mouse Basal Ganglia

  2021cites this paper
• Sim1-expressing cells illuminate the origin and course of migration of the nucleus of the lateral olfactory tract in the mouse amygdala

  2021cites this paper
• Differential expression of somatostatin genes in the central nervous system of the sea lamprey

  2021cites this paper
• The impact of (ab)normal maternal environment on cortical development.

  2021cites this paper
• Novel Perspectives on the Development of the Amygdala in Rodents

  2021cites this paper
• Genoarchitectonic Compartmentalization of the Embryonic Telencephalon: Insights From the Domestic Cat

  2021cites this paper
• The transcription factor TCF7L2 functions as a terminal selector in thalamic and habenular regions of the brain

  2020cites this paper
• Development of Limbic System Stress-Threat Circuitry

  2020cites this paper
• Topological atlas of the hypothalamus in adult rhesus monkey

  2020influential citation
• A radial histogenetic model of the mouse pallial amygdala

  2020cites this paper
• TCF7L2 regulates postmitotic differentiation programmes and excitability patterns in the thalamus

  2020cites this paper
• Developmental Genes and Malformations in the Hypothalamus

  2020influential citation
• LacZ‐reporter mapping of Dlx5/6 expression and genoarchitectural analysis of the postnatal mouse prethalamus

  2020cites this paper
• Developmental Neuroendocrinology

  2020cites this paper
• Histogenetic Radial Models as Aids to Understanding Complex Brain Structures: The Amygdalar Radial Model as a Recent Example

  2020cites this paper
• Longitudinal developmental analysis of prethalamic eminence derivatives in the chick by mapping of Tbr1 in situ expression

  2020cites this paper
• Neuronal tangential migration from Nkx2.1-positive hypothalamus

  2020cites this paper
• A novel telencephalon-opto-hypothalamic morphogenetic domain produces most of the glutamatergic neurons of the medial extended amygdala

  2020cites this paper
• Concentric ring topology of mammalian cortical sectors and relevance for patterning studies

  2019cites this paper
• TCF7L2 is a terminal selector that regulates postmitotic differentiation programs and excitability patterns in the thalamus

  2019cites this paper
• Patterned Vascularization of Embryonic Mouse Forebrain, and Neuromeric Topology of Major Human Subarachnoidal Arterial Branches: A Prosomeric Mapping

  2019cites this paper
• Hippocampal CA1 Somatostatin Interneurons Originate in the Embryonic MGE/POA

  2019cites this paper
• Differential expression of five prosomatostatin genes in the central nervous system of the catshark Scyliorhinus canicula

  2019cites this paper
• Survey of Midbrain, Diencephalon, and Hypothalamus Neuroanatomic Terms Whose Prosomeric Definition Conflicts With Columnar Tradition

  2019cites this paper
• The caudo-ventral pallium is a novel pallial domain expressing Gdf10 and generating Ebf3-positive neurons of the medial amygdala

  2018cites this paper
• Principles of Current Vertebrate Neuromorphology

  2017cites this paper
• A New Mammalian Brain Ontology Based on Developmental Gene Expression

  2017cites this paper
• Development of the hypothalamus: conservation, modification and innovation

  2017cites this paper
• Rostro-Caudal and Caudo-Rostral Migrations in the Telencephalon: Going Forward or Backward?

  2017cites this paper
• 1.23 – The Amygdala

  2017cites this paper
• Molecular control of two novel migratory paths for CGE-derived interneurons in the developing mouse brain

  2016cites this paper
• Subpallial Enhancer Transgenic Lines: a Data and Tool Resource to Study Transcriptional Regulation of GABAergic Cell Fate.

  2016cites this paper
• Radial derivatives of the mouse ventral pallium traced with Dbx1-LacZ reporters.

  2016cites this paper
• TCF7L2 regulates postmitotic differentiation programs and excitability patterns in the thalamus Abbreviated title TCF7L2 is a terminal selector in the thalamus Authors

  year unknowncites this paper