Aberrant survival of hippocampal Cajal-Retzius cells leads to memory deficits, gamma rhythmopathies and susceptibility to seizures in adult mice

Martina Riva, Stéphanie Moriceau, Annunziato Morabito, Elena Dossi, Candela Sanchez-Bellot, Patrick Azzam, Andrea Navas-Olive, Beatriz Gal, Francesco Dori, Elena Cid, Fanny Ledonne, Sabrina David, Fabrice Trovero, Magali Bartolomucci, Eva Coppola, Nelson Rebola, Antoine Depaulis, Nathalie Rouach, Liset Menendez Prida, Franck Oury and Alessandra Pierani ()
Additional contact information
Martina Riva: Université Paris Cité, Imagine Institute, Team Genetics and Development of the Cerebral Cortex
Stéphanie Moriceau: Platform for Neurobehavioral and metabolism, Structure Fédérative de Recherche Necker, 26 INSERM US24/CNRS UAR
Annunziato Morabito: Sorbonne Université, Institut Du Cerveau-Paris Brain Institute-ICM, Inserm U1127, CNRS UMR 7225
Elena Dossi: Université PSL
Candela Sanchez-Bellot: Instituto Cajal, CSIC
Patrick Azzam: Université Paris Cité, Imagine Institute, Team Genetics and Development of the Cerebral Cortex
Andrea Navas-Olive: Instituto Cajal, CSIC
Beatriz Gal: Instituto Cajal, CSIC
Francesco Dori: Université Paris Cité, Imagine Institute, Team Genetics and Development of the Cerebral Cortex
Elena Cid: Instituto Cajal, CSIC
Fanny Ledonne: Université Paris Cité, Institute of Psychiatry and Neuroscience of Paris, INSERM U1266
Sabrina David: Key-Obs SAS
Fabrice Trovero: Key-Obs SAS
Magali Bartolomucci: Université Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences
Eva Coppola: Université Paris Cité, Institute of Psychiatry and Neuroscience of Paris, INSERM U1266
Nelson Rebola: Sorbonne Université, Institut Du Cerveau-Paris Brain Institute-ICM, Inserm U1127, CNRS UMR 7225
Antoine Depaulis: Université Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences
Nathalie Rouach: Université PSL
Liset Menendez Prida: Instituto Cajal, CSIC
Franck Oury: Université Paris Cité, CNRS, INSERM, Institut Necker Enfants Malades-INEM
Alessandra Pierani: Université Paris Cité, Imagine Institute, Team Genetics and Development of the Cerebral Cortex

Nature Communications, 2023, vol. 14, issue 1, 1-21

Abstract: Abstract Cajal-Retzius cells (CRs) are transient neurons, disappearing almost completely in the postnatal neocortex by programmed cell death (PCD), with a percentage surviving up to adulthood in the hippocampus. Here, we evaluate CR’s role in the establishment of adult neuronal and cognitive function using a mouse model preventing Bax-dependent PCD. CRs abnormal survival resulted in impairment of hippocampus-dependent memory, associated in vivo with attenuated theta oscillations and enhanced gamma activity in the dorsal CA1. At the cellular level, we observed transient changes in the number of NPY+ cells and altered CA1 pyramidal cell spine density. At the synaptic level, these changes translated into enhanced inhibitory currents in hippocampal pyramidal cells. Finally, adult mutants displayed an increased susceptibility to lethal tonic-clonic seizures in a kainate model of epilepsy. Our data reveal that aberrant survival of a small proportion of postnatal hippocampal CRs results in cognitive deficits and epilepsy-prone phenotypes in adulthood.

Date: 2023
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DOI: 10.1038/s41467-023-37249-7

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