Developmental Cajal-Retzius cell death contributes to the maturation of layer 1 cortical inhibition and somatosensory processing

Angeliki Damilou, Linbi Cai, Ali Özgür Argunşah, Shuting Han, George Kanatouris, Maria Karatsoli, Olivia Hanley, Lorenzo Gesuita, Sepp Kollmorgen, Fritjof Helmchen and Theofanis Karayannis ()
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Angeliki Damilou: University of Zurich
Linbi Cai: University of Zurich
Ali Özgür Argunşah: University of Zurich
Shuting Han: Neuroscience Center Zurich
George Kanatouris: University of Zurich
Maria Karatsoli: University of Zurich
Olivia Hanley: University of Zurich
Lorenzo Gesuita: University of Zurich
Sepp Kollmorgen: University of Zürich
Fritjof Helmchen: University of Zürich
Theofanis Karayannis: University of Zurich

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract The role of developmental cell death in the formation of brain circuits is not well understood. Cajal-Retzius cells constitute a major transient neuronal population in the mammalian neocortex, which largely disappears at the time of postnatal somatosensory maturation. In this study, we used mouse genetics, anatomical, functional, and behavioral approaches to explore the impact of the early postnatal death of Cajal-Retzius cells in the maturation of the cortical circuit. We find that before their death, Cajal-Retzius cells mainly receive inputs from layer 1 neurons, which can only develop their mature connectivity onto layer 2/3 pyramidal cells after Cajal-Retzius cells disappear. This developmental connectivity progression from layer 1 GABAergic to layer 2/3 pyramidal cells regulates sensory-driven inhibition within, and more so, across cortical columns. Here we show that Cajal-Retzius cell death prevention leads to layer 2/3 hyper-excitability, delayed learning and reduced performance in a multi-whisker-dependent texture discrimination task.

Date: 2024
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DOI: 10.1038/s41467-024-50658-6

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