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Circadian Modulation of Neurons and Astrocytes Controls Synaptic Plasticity in Hippocampal Area CA1

Authors: John P. McCauley1, Maurice A. Petroccione1, Lianna Y. D’Brant1,2, Gabrielle C. Todd1, Nurat Affinnih1, Justin J. Wisnoski1, Shergil Zahid1, Swasti Shree1,3, Alioscka A. Sousa4,5, Rose M. De Guzman6, Rosanna Migliore7, Alexey Brazhe8,9, Richard D. Leapman5, Alexander Khmaladze2, Alexey Semyanov9,10, Damian G. Zuloaga6, Michele Migliore,7, and Annalisa Scimemi1

Author information: 1Department of Biology, SUNY Albany, 1400 Washington Avenue, Albany, NY 12222, USA, 2 Department of Physics, SUNY Albany, 1400 Washington Avenue, Albany, NY 12222, USA, 3 Bethlehem Central High School, 700 Delaware Avenue, Delmar, NY 12054, USA, 4 Federal University of Sao Paulo, Department of Biochemistry, 100 Rua Tres de Maio, Sao Paulo 04044-020, Brazil, 5 National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, 9000 Rockville Pike, Bethesda, MD 20892, USA, 6 Department of Psychology, SUNY Albany, 1400 Washington Avenue, Albany, NY 12222, USA, 7 Institute of Biophysics, National Research Council, 153 Via Ugo La Malfa, Palermo 90146, Italy, 8 Department of Biophysics, Lomonosov Moscow State University, Leninskie Gory 1/12, Moscow 119234, Russia, 9 Department of Molecular Neurobiology, Institute of Bioorganic Chemistry, Ulitsa Miklukho-Maklaya 16/10, Moscow 117997, Russia, 10Sechenov First Moscow State Medical University, Bolshaya Pirogovskaya Ulitsa 19s1, Moscow 119146, Russia.

Corresponding author: (Annalisa Scimemi ascimemi@albany.edu )

Journal: Cell Reports

Download Url: https://www.cell.com/cell-reports/fulltext/S2211-1247(20)31244-4

Citation: McCauley et al., Cell Reports 33, 108255, 2020.

DOI: https://doi.org/10.1016/j.celrep.2020.108255

Licence: the Creative Commons Attribution (CC BY) license  applies for all files. Under this Open Access license anyone  may copy, distribute, or reuse the files as long as the authors and the original source are properly cited.

Abstract:
Most animal species operate according to a 24-h period set by the suprachiasmatic nucleus (SCN) of the hypothalamus. The rhythmic activity of the SCNmodulates hippocampal-dependent memory, but the molecular and cellular mechanisms that account for this effect remain largely unknown. Here, we identify cell-typespecific structural and functional changes that occur with circadian rhythmicity in neurons and astrocytes in hippocampal area CA1. Pyramidal neurons change the surface expression of NMDA receptors. Astrocytes change their proximity to synapses. Together, these phenomena alter glutamate clearance, receptor activation, and integration of temporally clustered excitatory synaptic inputs, ultimately shaping hippocampaldependent learning in vivo. We identify corticosterone as a key contributor to changes in synaptic strength. These findings highlight important mechanisms through which neurons and astrocytes modify the molecular composition and structure of the synaptic environment, contribute to the local storage of information in the hippocampus, and alter the temporal dynamics of cognitive processing.
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Data and models: data and models used in the paper are available at the links reported below.