Reallocation of Olfactory Cajal-Retzius Cells Shapes Neocortex Architecture.
The neocortex undergoes extensive developmental growth, but how its architecture adapts to expansion remains largely unknown. Here, we investigated how early born Cajal-Retzius (CR) neurons, which regulate the assembly of cortical circuits, maintain a dense superficial distribution in the growing neocortex. We found that CR cell density is sustained by an activity-dependent importation of olfactory CR cells, which migrate into the neocortex after they have acted as axonal guidepost cells in the olfactory system. Furthermore, using mouse genetics, we showed that CR cell density severely affects the architecture of layer 1, a key site of input integration for neocortical networks, leading to an excitation/inhibition ratio imbalance. Our study reveals that neurons reenter migration several days after their initial positioning, thereby performing sequential developmental roles in olfactory cortex and neocortex. This atypical process is essential to regulate CR cell density during growth, which in turn ensures the correct wiring of neocortical circuitry. VIDEO ABSTRACT.
Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l'ENS (IBENS), INSERM, CNRS, Brain Development and Plasticity Team, F-75005 Paris, France.
Cristina A
CA
de Frutos
Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l'ENS (IBENS), INSERM, CNRS, Cerebellum Team, F-75005 Paris, France.
Guy
G
Bouvier
Institut Jacques Monod, CNRS UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, 75205 Paris Cedex, France.
Yoko
Y
Arai
Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l'ENS (IBENS), INSERM, CNRS, Brain Development and Plasticity Team, F-75005 Paris, France.
Morgane S
MS
Thion
Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l'ENS (IBENS), INSERM, CNRS, Brain Development and Plasticity Team, F-75005 Paris, France.
Ludmilla
L
Lokmane
Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l'ENS (IBENS), INSERM, CNRS, Brain Development and Plasticity Team, F-75005 Paris, France.
Maryama
M
Keita
Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l'ENS (IBENS), INSERM, CNRS, Nervous System Development Team, F-75005 Paris, France; Stem Cells, CABIMER (CSIC), 41092 Seville, Spain.
Mario
M
Garcia-Dominguez
Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l'ENS (IBENS), INSERM, CNRS, Nervous System Development Team, F-75005 Paris, France.
Patrick
P
Charnay
Division of Brain Function, National Institute of Genetics, Mishima 411-8540, Japan.
Tatsumi
T
Hirata
Department of Biomedical Sciences, School of Medicine, Nazarbayev University, Astana 010000, Kazakhstan.
Dieter
D
Riethmacher
Department of Neurobiology, University of Chicago, Chicago, IL 60637, USA.
Elizabeth A
EA
Grove
Developmental Neurobiology Unit, Institute of Neuroscience, University of Louvain, 1348 Brussels, Belgium.
Fadel
F
Tissir
Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l'ENS (IBENS), INSERM, CNRS, Cerebellum Team, F-75005 Paris, France.
Mariano
M
Casado
Institut Jacques Monod, CNRS UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, 75205 Paris Cedex, France.
Alessandra
A
Pierani
Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l'ENS (IBENS), INSERM, CNRS, Brain Development and Plasticity Team, F-75005 Paris, France. Electronic address: garel@biologie.ens.fr.
Sonia
S
Garel
D000818:Animals; D001369:Axons; D002452:Cell Count; D002465:Cell Movement; D007395:Interneurons / Q000502:physiology; D051379:Mice; D019579:Neocortex / Q000196:embryology*; D009474:Neurons / Q000502:physiology*; D009830:Olfactory Bulb / Q000166:cytology / Q000196:embryology*; D066194:Olfactory Cortex / Q000196:embryology*
Cajal-Retzius cells; E/I ratio; NMDA receptors; interneurons; layer 1; marginal zone; migration; neocortex; olfactory cortex