Sleep differentially modulates synaptic vesicle protein 2A and spine density across cortical regions and development

iScience, vol. 29, pp. 116676

Abstract

Sleep is proposed to regulate synaptic strength; yet, the underlying mechanisms remain debated under the synaptic homeostasis hypothesis (SHY). We examined synaptic vesicle glycoprotein 2A (SV2A) and dendritic spine density in mouse brain across conditions of physiological sleep and sleep deprivation. Spine density decreased during sleep and increased following sleep deprivation, consistent with the SHY. In contrast, [ 18 F]SynVesT-1 positron emission tomography (PET) imaging and [ 3 H]UCB-J autoradiography revealed reduced SV2A following sleep deprivation. Layer-specific analyses in somatosensory and visual cortices further supported coordinated regulation between SV2A and dendritic spines. Developmentally, adolescent mice exhibited higher baseline SV2A and spine density than adults, with greater SV2A sensitivity to sleep deprivation, whereas adults were more responsive to physiological sleep. Together, these findings reveal bidirectional regulation of pre- and postsynaptic compartments and highlight developmental differences in sleep-dependent synaptic organization.

Authors 18

1. Jing Ma Aachen Systems Neurophysiology Institute of Zoology (Biology 2)

   Forschungszentrum Jülich · RWTH Aachen University

   Affiliation as printed

   Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

   Systems Neurophysiology, Institute of Zoology, RWTH Aachen University, Aachen, Germany

2. Alexandra Braun

   Forschungszentrum Jülich

   Affiliation as printed

   Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

3. Angela Oskamp

   Forschungszentrum Jülich

   Affiliation as printed

   Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

4. Lena Kricsfalussy-Hrabár Aachen Systems Neurophysiology Institute of Zoology (Biology 2)

   Forschungszentrum Jülich · RWTH Aachen University

   Affiliation as printed

   Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

   Systems Neurophysiology, Institute of Zoology, RWTH Aachen University, Aachen, Germany

5. Nadja Hermes

   Forschungszentrum Jülich

   Affiliation as printed

   Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

6. Salma Djakkani

   Forschungszentrum Jülich

   Affiliation as printed

   Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

7. Ulrike Holz

   Forschungszentrum Jülich

   Affiliation as printed

   Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

8. Sabine Jakobs

   Forschungszentrum Jülich

   Affiliation as printed

   Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

9. Sabina Klein

   Forschungszentrum Jülich

   Affiliation as printed

   Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

10. Stefan Stüsgen

    Forschungszentrum Jülich

    Affiliation as printed

    Institute of Neuroscience and Medicine, Nuclear Chemistry (INM-5), Forschungszentrum Jülich, Jülich, Germany

11. Philipp Krapf

    Forschungszentrum Jülich

    Affiliation as printed

    Institute of Neuroscience and Medicine, Nuclear Chemistry (INM-5), Forschungszentrum Jülich, Jülich, Germany

12. Bernd Neumaier

    Forschungszentrum Jülich

    Affiliation as printed

    Institute of Neuroscience and Medicine, Nuclear Chemistry (INM-5), Forschungszentrum Jülich, Jülich, Germany

13. Alexander E. Drzezga

    Forschungszentrum Jülich · University of Cologne · German Center for Neurodegenerative Diseases · University Hospital Cologne

    Affiliation as printed

    Department of Nuclear Medicine, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany

    German Center for Neurodegenerative Diseases (DZNE), Bonn-Cologne, Germany

    Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

14. Simone Beer

    Forschungszentrum Jülich

    Affiliation as printed

    Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

15. Andreas Bauer

    Forschungszentrum Jülich · Heinrich Heine University Düsseldorf

    Affiliation as printed

    Department of Neurology, Medical Faculty, Heinrich-Heine-University Düsseldorf, 40225 Düsseldorf, Germany

    Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany

16. Astrid Rollenhagen

    Forschungszentrum Jülich · Jülich Aachen Research Alliance

    Affiliation as printed

    JARA BRAIN, Institute of Neuroscience and Medicine (INM-10), Forschungszentrum Jülich, Jülich, Germany

17. Björn M. Kampa Aachen Systems Neurophysiology Institute of Zoology (Biology 2)

    Forschungszentrum Jülich · Jülich Aachen Research Alliance · RWTH Aachen University

    Affiliation as printed

    JARA BRAIN, Institute of Neuroscience and Medicine (INM-10), Forschungszentrum Jülich, Jülich, Germany

    Systems Neurophysiology, Institute of Zoology, RWTH Aachen University, Aachen, Germany

18. David Elmenhorst corresponding

    Forschungszentrum Jülich · University of Cologne · University Hospital Cologne

    Affiliation as printed

    Department of Nuclear Medicine, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany

    Institute of Neurosciences and Medicine, Molecular Organization of the Brain (INM-2), Forschungszentrum Jülich, Jülich, Germany