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

Author

Listed:
  • Martina Riva

    (Université Paris Cité, Imagine Institute, Team Genetics and Development of the Cerebral Cortex
    Université Paris Cité, Institute of Psychiatry and Neuroscience of Paris, INSERM U1266)

  • 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
    Université Paris Cité, Institute of Psychiatry and Neuroscience of Paris, INSERM U1266)

  • Andrea Navas-Olive

    (Instituto Cajal, CSIC)

  • Beatriz Gal

    (Instituto Cajal, CSIC
    Universidad Camilo José Cela)

  • Francesco Dori

    (Université Paris Cité, Imagine Institute, Team Genetics and Development of the Cerebral Cortex
    Université Paris Cité, Institute of Psychiatry and Neuroscience of Paris, INSERM U1266)

  • 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
    Université Paris Cité, Institute of Psychiatry and Neuroscience of Paris, INSERM U1266
    Hôpital Sainte Anne)

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.

Suggested Citation

  • 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, 2023. "Aberrant survival of hippocampal Cajal-Retzius cells leads to memory deficits, gamma rhythmopathies and susceptibility to seizures in adult mice," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37249-7
    DOI: 10.1038/s41467-023-37249-7
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    References listed on IDEAS

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    1. José A. Del Río & Bernd Heimrich & Víctor Borrell & Eckart Förster & Alexander Drakew & Soledad Alcántara & Kazunori Nakajima & Takaki Miyata & Masaharu Ogawa & Katsuhiko Mikoshiba & Paul Derer & Mich, 1997. "A role for Cajal–Retzius cells and reelin in the development of hippocampal connections," Nature, Nature, vol. 385(6611), pages 70-74, January.
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    1. Andrea Zanetti & Gwendal Dujardin & Lucas Fares-Taie & Jeanne Amiel & Jérôme E. Roger & Isabelle Audo & Matthieu P. Robert & Pierre David & Vincent Jung & Nicolas Goudin & Ida Chiara Guerrera & Stépha, 2024. "GPATCH11 variants cause mis-splicing and early-onset retinal dystrophy with neurological impairment," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

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