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

Ioana Genescu (1) , Mar Aníbal-Martínez (2) , Vladimir Kouskoff (3) , Nicolas Chenouard (3) , Caroline Mailhes-Hamon (1) , Hugues Cartonnet (1) , Ludmilla Lokmane (1) , Filippo Rijli (4) , Guillermina López-Bendito (2) , Frédéric Gambino (3) , S. Garel (1, 5)

1 IBENS - Institut de biologie de l'ENS Paris
2 Instituto de Neurociencias de Alicante
3 IINS - Interdisciplinary Institute for Neuroscience [Bordeaux]
4 FMI - Friedrich Miescher Institute for Biomedical Research
5 Collège de France - Chaire Neurobiologie et immunité

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.

Domains: Neurobiology; Embryology and Organogenesis

Ioana Genescu, Mar Aníbal-Martínez, Vladimir Kouskoff, Nicolas Chenouard, Caroline Mailhes-Hamon, et al.. Dynamic interplay between thalamic activity and Cajal-Retzius cells regulates the wiring of cortical layer 1. Cell Reports, 2022, 39 (2), pp.110667. ⟨10.1016/j.celrep.2022.110667⟩. ⟨hal-03651820⟩