Acute Inescapable Stress Rapidly Increases Synaptic Energy Metabolism in Prefrontal Cortex and Alters Working Memory Performance

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DOI

  • Laura Musazzi, Laboratory of Neuropsychopharmacology and Functional Neurogenomics, Dipartimento di Scienze Farmacologiche e Biomolecolari, Center of Excellence on Neurodegenerative Diseases (CEND), Università degli Studi di Milano , Milano , Italy.
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  • Nathalie Sala, Laboratory of Neuropsychopharmacology and Functional Neurogenomics, Dipartimento di Scienze Farmacologiche e Biomolecolari, Center of Excellence on Neurodegenerative Diseases (CEND), Università degli Studi di Milano , Milano , Italy.
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  • Paolo Tornese, Laboratory of Neuropsychopharmacology and Functional Neurogenomics, Dipartimento di Scienze Farmacologiche e Biomolecolari, Center of Excellence on Neurodegenerative Diseases (CEND), Università degli Studi di Milano , Milano , Italy.
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  • Francesca Gallivanone, Institute of Molecular Bioimaging and Physiology (IBFM), Milan Center for Neuroscience (NeuroMi) CNR, Segrate, Italy.
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  • Sara Belloli, Institute of Molecular Bioimaging and Physiology (IBFM), Milan Center for Neuroscience (NeuroMi) CNR, Segrate, Italy.
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  • Alessandra Conte, Laboratory of Neuropsychopharmacology and Functional Neurogenomics, Dipartimento di Scienze Farmacologiche e Biomolecolari, Center of Excellence on Neurodegenerative Diseases (CEND), Università degli Studi di Milano , Milano , Italy.
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  • Giuseppe Di Grigoli, Institute of Molecular Bioimaging and Physiology (IBFM), Milan Center for Neuroscience (NeuroMi) CNR, Segrate, Italy.
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  • Fengua Chen, 1. Translational Neuropsychiatry Unit, Department of Clinical Medicine, Aarhus University Hospital, Risskov, Denmark.
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  • Ayşe Ikinci, Department of Clinical Medicine, Core Centre for Molecular Morphology, Section for Stereology and Microscopy, Aarhus University Hospital, Aarhus C, Denmark.
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  • Giulia Treccani
  • Chiara Bazzini, Laboratory of Neuropsychopharmacology and Functional Neurogenomics, Dipartimento di Scienze Farmacologiche e Biomolecolari, Center of Excellence on Neurodegenerative Diseases (CEND), Università degli Studi di Milano , Milano , Italy.
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  • Isabella Castiglioni, Institute of Molecular Bioimaging and Physiology (IBFM), Milan Center for Neuroscience (NeuroMi) CNR, Segrate, Italy.
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  • Jens R Nyengaard
  • Gregers Wegener
  • Rosa M Moresco, Department of Medicine and Surgery, University of Milan Bicocca, Monza, Italy.
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  • Maurizio Popoli, Laboratory of Neuropsychopharmacology and Functional Neurogenomics, Dipartimento di Scienze Farmacologiche e Biomolecolari, Center of Excellence on Neurodegenerative Diseases (CEND), Università degli Studi di Milano , Milano , Italy.

Brain energy metabolism actively regulates synaptic transmission and activity. We have previously shown that acute footshock (FS)-stress induces fast and long-lasting functional and morphological changes at excitatory synapses in prefrontal cortex (PFC). Here, we asked whether FS-stress increased energy metabolism in PFC, and modified related cognitive functions. Using positron emission tomography (PET), we found that FS-stress induced a redistribution of glucose metabolism in the brain, with relative decrease of [18F]FDG uptake in ventro-caudal regions and increase in dorso-rostral ones. Absolute [18F]FDG uptake was inversely correlated with serum corticosterone. Increased specific hexokinase activity was also measured in purified PFC synaptosomes (but not in total extract) of FS-stressed rats, which positively correlated with 2-Deoxy [3H] glucose uptake by synaptosomes. In line with increased synaptic energy demand, using an electron microscopy-based stereological approach, we found that acute stress induced a redistribution of mitochondria at excitatory synapses, together with an increase in their volume. The fast functional and metabolic activation of PFC induced by acute stress, was accompanied by rapid and sustained alterations of working memory performance in delayed response to T-maze test. Taken together, the present data suggest that acute stress increases energy consumption at PFC synaptic terminals and alters working memory.

Original languageEnglish
JournalCerebral Cortex
ISSN1047-3211
DOIs
Publication statusE-pub ahead of print - 16 Mar 2019
Externally publishedYes

Bibliographical note

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