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Roles of Cajal-Retzius Cells Ioana Genescu Assembling layer 1 of the neocortex : roles of Cajal-Retzius cells Ioana Genescu To cite this version: Ioana Genescu. Assembling layer 1 of the neocortex : roles of Cajal-Retzius cells. Neurons and Cognition [q-bio.NC]. Université Paris sciences et lettres, 2020. English. NNT : 2020UPSLE007. tel-03188109 HAL Id: tel-03188109 https://tel.archives-ouvertes.fr/tel-03188109 Submitted on 1 Apr 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Préparée à l’Institut de Biologie de l’École Normale Supérieure L'assemblage de la couche 1 du néocortex : Rôles des cellules de Cajal-Retzius Assembling layer 1 of the neocortex: Roles of Cajal-Retzius cells Soutenue par Composition du jury : Ioana GENESCU Patricia, GASPAR Le 08 octobre 2020 DR, Institut du Cerveau, Paris Présidente Alain, CHÉDOTAL DR, Institut de la Vision, Paris Rapporteur Ecole doctorale n° 515 Denis, JABAUDON Prof., Université de Genève, Genève Rapporteur Complexité du Vivant Alexandre, BAFFET CR., Institut Curie, Paris Examinateur Alessandra, PIERANI DR., Institut Imagine, IPNP, Paris Examinatrice Spécialité Sonia, GAREL Neurosciences Prof., IBENS, Collège de France, Paris Directrice de thèse Biologie du développement TABLE OF CONTENTS LIST OF ABBREVIATIONS 10 INTRODUCTION 14 Preablme 15 1. Overview of the cerebral cortex 16 1.1 Neuronal composition of the neocortex 16 1.2 Architecture of the neocortex: areas, connectivity, layers and columns 16 1.2.1 Organization of the neocortex: tangential in layers, radial in columns 17 1.2.2 Bottom-up information processing 19 1.2.3 Top-down information processing 20 1.3 Layer 1: an atypical layer of the neocortex 21 1.3.1 Anatomy of neocortical layer 1 in adults 21 1.3.1.a Cellular composition 21 1.3.1.b Axonal and dendritic composition 24 1.3.2 Layer 1 in adult neocortical functions 26 2. Developmental programs in the neocortex and layer 1 formation 29 2.1 General overview of telencephalic development 29 2.2 Generation and migration of cortical neurons 32 2.2.1 Generation and migration of Cajal-Retzius cells 32 2.2.2 Generation and migration of Subplate neurons 34 2.2.3 Generation and migration of Pyramidal neurons 35 2.2.3.a Subtypes of pyramidal neurons and their progenitors 35 2.2.3.b Migration and morphological differentiation of pyramidal neurons 36 2.2.4 Generation and migration of Interneurons 40 2.2.4.a Origin of interneurons and link to their diversity 40 2.2.4.b Migration and positioning of interneurons in the neocortex 43 2.3 Construction of neocortical layer 1 43 2.3.1 Cellular components of the developing neocortical layer 1 43 2.3.2 Axonal components of the developing neocortical layer 1 44 3. Roles of electrical activity in the development of neocortical circuits 48 3.1 Early activity in shaping the formation of cortical circuits 48 3.2 Patterns of electrical activity in neocortical maturation 51 4. Programs and electrical activity in neocortical cell death 53 4.1 Programmed cell death in developing neocortex 53 4.1.1 Substantial elimination of transient neuronal populations 54 4.1.2 A coordinated downsizing of excitatory and inhibitory neuronal populations 55 4.2 Electrical activity regulates the death of neocortical neurons 57 5. Key regulators of neocortical layer 1 wiring: Cajal-Retzius cells 59 5.1 Morphological and molecular characterization of Cajal-Retzius cells 59 5.2 Cajal-Retzius cells are embedded in functional circuits 60 5.3 Functions of Cajal-Retzius cells in the wiring of upper cortical layers 62 5.4 Cajal-Retzius cells in human neocortical development 64 5.5 Potential roles of Cajal-Retzius cells and Reelin in neurodevelopmental disorders 65 RESULTS 68 Article 1 70 Activity-dependent death of Cajal-Retzius neurons is required for functional cortical wiring Article 2 94 Layer 1 wiring is shaped by Cajal-Retzius cells and early sensory activity Review 126 Being superficial: A developmental viewpoint on cortical layer 1 wiring DISCUSSION AND CONCLUSIONS 150 1. Neuronal acitivity in life and death of Cajal-Retzius cells 152 1.1 Cajal-Retzius cell density is shaped by two different activity dependent phases 152 1.2 By which mechanisms activity modulates Cajal-Retzius cell density ? 153 1.2.1 Cajal-Retzius cells redistribution 153 1.2.2 Cajal-Retzius cells elimination 154 2. All Cajal-Retzius cells are not born equal 157 3. Cajal-Retzius cells regulate the excitation/inhibition balance of the neocortex 160 3.1 Cajal-Retzius cells impact on the density of specific subpopulations of interneurons 160 3.1.1 Early impact of Cajal-Retzius cell density on interneurons 160 3.1.2 Long-lasting impact of Cajal-Retzius cell density on interneurons 162 3.2 Cajal-Retzius cells regulate excitatory inputs in layer 1 164 3.2.1 Do Cajal-Retzius have a general impact on branching and spine formation in layer 1? 164 3.2.2 Through which mechanisms coud Cajal-Retzius cells act? 166 3.2.3 Are Cajal-Retzius cells modulating excitatory axonal inputs in neocortical layer 1? 167 4. Cajal-Retzius cells and evolution 170 General conclusion 171 ANNEXES 172 Resumé de thèse 173 REFERENCES 178 TABLE OF FIGURES Figure 1 | Organization of the neocortex: tangential in layers, radial in columns 18 Figure 2 | Connectivity in the somatosensory cortex 21 Figure 3 | Interneuron subtypes across cortical layers 22 Figure 4 | Interneuron subtypes in adult cortical layer 1 23 Figure 5 | Layer 1 is a major site of input integration 26 Figure 6 | Connectivity motifs in cortical networks 28 Figure 7 | Development of pallium and acquisition of cortical areal identity 31 Figure 8 | Generation and distribution of pyramidal neurons 39 Figure 9 | Origin and main classes of interneurons 41 Figure 10 | Timeline of layer 1 development 47 Figure 11 | Emergence of activity in the developing cortex 52 Figure 12 | Developmental timeline of cell death in the neocortex 56 Figure 13 | Interplay between electrical activity and neuronal apoptosis in developing cortex 58 Figure 14 | Morphology of Cajal-Retzius cells in neocortical layer 1 60 Figure 15 | Input/output connectivity of Cajal-Retzius cells 62 Figure 16 | Cajal-Retzius cell density is in part modulated by activity dependent mechanisms 152 Figure 17 | Most SE and ET-derived Cajal-Retzius cells die in an activity-dependent manner 158 Figure 18 | Decreased Cajal-Retzius cell density is not impacting Martinotti cells axons 162 Figure 19 | Impact of Cajal-Retzius cell density on the CGE and POA-derived interneurons 163 Figure 20 | Impact of Cajal-Retzius cell density on the apical dendrites 165 Figure 21 | Cajal-Retzius cell density impacts on axonal plexus in layer 1 168 Figure 22 | The theory of neocortical cytoarchitectonics 170 LIST OF ABBREVIATIONS 5HT3R Serotonin receptor 3A A1 Primary Auditory cortex AIS axon initial segment AMPA α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid AMPAr AMPA receptors AP antero-posterior ApoER2 Apolipoprotein E receptor 2 ASD Autistic Spectrum Disorders Bak Bcl2 antagonist/killer 1 Bax Bcl2 associated X protein BDNF Brain-Derived Neurotrophic Factor BMP Bone Morphogenic protein Casp Caspase Cbln4 Cerebellin 4 CC Corpus Callosum cENO cortical Early Network Oscillations CGE Caudal Ganglionic Emminence cKO conditional Knock-Out CNO Clozapine – N - oxide CNS Central Nervous System CoupTF1 NR2F1, COUP transcription factor 1 CoupTF2 Chicken ovalbumin upstream promoter-transcription factor 2 CP Cortical Plate CRc Cajal-Retzius cell Ctip2 Chicken ovalbumin upstream promoter transcription factor-interacting protein 2 Dab1 Disabled 1 Dbx1 Developing brain homeobox 1 Dlx Distal less homeobox DS Down Syndrome DV dorso-ventral E embryonic day E/I Excitation/Inhibition ratio Emx2 Empty spiracle homeobox 2 EPSC Excitatory postsynaptic currents Er81 Ets variant gene 1 Fezf2 FEZ family zinc finger 2 Fgf Fibroblast growth factor Fgf13 Fibroblast growth factor 13 GABA Gamma amino-butiric acid GDP Giant Depolarizing Potential GluN1 N-methyl-D-aspartate receptor subunit NR1 IGF Insulin Growth Factor Igf1 Insulin like growth factor 1 10 ION Infraorbital Nerve IPSC Inhibitory postsynaptic currents KCC2 Potassium-chloride transporter member 5 L1 Cortical layer 1 L2/3 Cortical layer 2/3 L4 Cortical layer 4 L5/6 Cortical layer 5/6 Lgi2 Leucine-rich repeat LGI family member 2 LOT Lateral Olfactory Tract M1 Primary Motor cortex MGE Medial Ganglionic Emminence MZ Marginal Zone NDNF Neuron Derived Neurotrophic Factor NGF Nerve Growth Factor NGFc Nurogliaform cells NKCC1 Na-K-Cl cotransporter isoform 1 NMDA Acid N-methyl-D-aspartic NMDAR NMDA receptors NPY Neuropeptide Y Nr2f2 Nuclear receptor subfamily 2 group F member 2 NT-3 Neurotrophin-3 NT-4 Neurotrophin-4 P postnatal day Pax6 Paired box gene 6 PCD Programmed Cell Death pCRc human persistent Cajal-Retzius cells PNS Peripheral Nervous System POA Preoptic Area Prox 1 Prospero homeobox 1 PrV Rostral principal nucleus in the brainstem PV Parvalbumin RA Retinoic Acid RELN Reelin protein RGc Radial glia cell S1 Primary Somatosensory cortex Satb2 Special AT-rich sequence-binding protein 2 SBc Single bouquet cells SE Septum Sema Semaphorin Shh Sonic Hedgehog
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