Dynamic interplay between thalamic activity and Cajal-Retzius cells regulates the wiring of cortical layer 1

• Published in: Cell reports (Cambridge) 2022-04, Vol.39 (2), p.110667-110667, Article 110667
• Main Authors: Genescu, Ioana, Aníbal-Martínez, Mar, Kouskoff, Vladimir, Chenouard, Nicolas, Mailhes-Hamon, Caroline, Cartonnet, Hugues, Lokmane, Ludmilla, Rijli, Filippo M., López-Bendito, Guillermina, Gambino, Frédéric, Garel, Sonia
• Format: Article
• Language: English
• Subjects: apical dendrites; Cajal-Retzius cells; cortical development; Dendrites - physiology; Development Biology; E/I ratio; Embryology and Organogenesis; interneurons; Interneurons - physiology; layer 1; Life Sciences; Neurobiology; Neurons - physiology; Neurons and Cognition; NMDA receptors; Pyramidal Cells; spines; spontaneous activity; Thalamus
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2022.110667

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. [Display omitted] •Prenatal thalamic waves of activity regulate CRc density in L1•Prenatal and postnatal CRc manipulations alter specific interneuron populations•Postnatal CRc shape L5 apical dendrite structural and functional properties•Early sensory activity selectively regulates L5 basal dendrite spine formation Genescu et al. show that the wiring of cortical layer 1 relies on crosstalk between spontaneous thalamic activity and Cajal-Retzius cells, with long-lasting consequences on cortical circuits. These findings reveal that transient activity and cells play key roles in the wiring of apical dendrites and upper layer neocortical networks.