Dynamic interplay between thalamic activity and Cajal-Retzius cells regulates the wiring of cortical layer 1
Cell Reports. 2022-04-01; 39(2): 110667
DOI: 10.1016/j.celrep.2022.110667
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Genescu I(1), Aníbal-Martínez M(2), Kouskoff V(3), Chenouard N(3), Mailhes-Hamon
C(4), Cartonnet H(1), Lokmane L(1), Rijli FM(5), López-Bendito G(2), Gambino
F(3), Garel S(6).
Author information:
(1)Institut de Biologie de l’École Normale Supérieure (IBENS), Département de
Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, 75005 Paris,
France.
(2)Instituto de Neurosciencias de Alicante, Universidad Miguel Hernandez, Sant
Joan d’Alacant, Spain.
(3)University of Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience,
IINS UMR 5297, 33000 Bordeaux, France.
(4)Acute Transgenesis Facility, Institut de Biologie de l’École Normale
Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, PSL Université
Paris, 75005 Paris, France.
(5)Friedrich Miescher Institute for Biomedical Research, 4058 Basel,
Switzerland; University of Basel, 4056 Basel, Switzerland.
(6)Institut de Biologie de l’École Normale Supérieure (IBENS), Département de
Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, 75005 Paris,
France; Collège de France, 75005 Paris, France. Electronic address:
.
Cortical wiring relies on guidepost cells and activity-dependent processes that
are thought to act sequentially. Here, we show that the construction of layer 1
(L1), a main site of top-down integration, is regulated by crosstalk between
transient Cajal-Retzius cells (CRc) and spontaneous activity of the thalamus, a
main driver of bottom-up information. While activity was known to regulate CRc
migration and elimination, we found that prenatal spontaneous thalamic activity
and NMDA receptors selectively control CRc early density, without affecting
their demise. CRc density, in turn, regulates the distribution of upper layer
interneurons and excitatory synapses, thereby drastically impairing the apical
dendrite activity of output pyramidal neurons. In contrast, postnatal
sensory-evoked activity had a limited impact on L1 and selectively perturbed
basal dendrites synaptogenesis. Collectively, our study highlights a remarkable
interplay between thalamic activity and CRc in L1 functional wiring, with major
implications for our understanding of cortical development.
Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.
Conflict of interest statement: Declaration of interests The authors declare no
competing interests.