TY - JOUR
T1 - Acute Inescapable Stress Rapidly Increases Synaptic Energy Metabolism in Prefrontal Cortex and Alters Working Memory Performance
AU - Musazzi, Laura
AU - Sala, Nathalie
AU - Tornese, Paolo
AU - Gallivanone, Francesca
AU - Belloli, Sara
AU - Conte, Alessandra
AU - Di Grigoli, Giuseppe
AU - Chen, Fenghua
AU - Ikinci, Ayşe
AU - Treccani, Giulia
AU - Bazzini, Chiara
AU - Castiglioni, Isabella
AU - Nyengaard, Jens R
AU - Wegener, Gregers
AU - Moresco, Rosa M
AU - Popoli, Maurizio
N1 - © The Author(s) 2019. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: [email protected].
PY - 2019/12
Y1 - 2019/12
N2 - 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.
AB - 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.
KW - acute stress
KW - brain metabolism
KW - positron emission tomography
KW - prefrontal cortex
KW - rat
U2 - 10.1093/cercor/bhz034
DO - 10.1093/cercor/bhz034
M3 - Journal article
C2 - 30877789
SN - 1047-3211
VL - 29
SP - 4948
EP - 4957
JO - Cerebral Cortex
JF - Cerebral Cortex
IS - 12
ER -