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Acute stress rapidly increases the readily releasable pool of glutamate vesicles in prefrontal and frontal cortex through non-genomic action of corticosterone

Molecular Psychiatry volume 19, page 401 (2014)Cite this article

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The rise of corticosterone (CORT) induced by acute stress causes in synaptic terminals of prefrontal and frontal cortex a rapid increase of vesicle trafficking into the readily releasable pool (RRP) of glutamate vesicles, with consequent increase of RRP size. This requires binding of CORT to (putatively) membrane-associated synaptic mineralocorticoid/glucocorticoid receptor and non-genomic mechanisms, involving phosphorylation of the presynaptic protein synapsin I. We have shown previously that acute stress enhances depolarization-dependent glutamate release.1 However, we found here that the increase of RRP size rapidly induced by CORT primes the terminal but is not sufficient for the enhancement of glutamate release. Indeed, in vitro incubation of purified synaptic terminals (synaptosomes) with CORT rapidly increases the size of glutamate RRP but does not increase glutamate release. Similarly, application in vitro of CORT to brain slices for up to 20 min does not increase synaptic transmission in prefrontal cortex. We speculate that slower (>20 min), likely genomic effects are required to promote the enhancement of glutamate release and transmission induced by acute stress. In line with this hypothesis, it has been shown previously that acute in vitro treatment of prefrontal cortex slices induces synaptic potentiation at least 1 h after CORT application, suggesting that the CORT-mediated enhancement of transmission in this area requires at least 1 h.2 For more information on this topic, please refer to the article by Treccani et al. on pages 433–443.

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References

  1. Musazzi L, Milanese M, Barbiero VS, Zappettini S, Tardito D, Farisello P et al. Acute stress increases depolarization-evoked glutamate release in the rat prefrontal/frontal cortex. The dampening action of antidepressants. PloS ONE 2010; 5: e8566.

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Authors and Affiliations

  1. Dipartimento di Scienze Farmacologiche e Biomolecolari and CEND, Laboratory of Neuropsychopharmacology and Functional Neurogenomics, Università di Milano, Milano, Italy

    G Treccani, L Musazzi, G Racagni & M Popoli

  2. Dipartimento di Scienze Farmacologiche e Biomolecolari, Laboratory of Cell Physiology, Università di Milano, Milano, Italy

    C Perego

  3. Department of Pharmacy, Unit of Pharmacology and Toxicology, Center of Excellence for Biomedical Research, Università di Genova, Genova, Italy

    M Milanese, T Bonifacino & G Bonanno

  4. Stereology and Electron Microscopy Laboratory, Centre for Stochastic Geometry and Advanced Bioimaging, Aarhus University Hospital, Aarhus C, Denmark

    N Nava & J R Nyengaard

  5. Centre for Psychiatric Research, Aarhus University Hospital, Risskov, Denmark

    N Nava & G Wegener

  6. Neurobiology of Learning Unit, Scientific Institute San Raffaele and Università Vita e Salute San Raffaele, Milano, Italy

    J Lamanna & A Malgaroli

  7. Department of Clinical and Molecular Biomedicine, Section of Pharmacology and Biochemistry, Università di Catania, Catania, Italy

    F Drago

  8. I.R.C.C.S San Giovanni di Dio-Fatebenefratelli, Brescia, Italy

    G Racagni

  9. Pharmaceutical Research Center of Excellence, School of Pharmacy (Pharmacology), North-West University, Potchefstroom, South Africa

    G Wegener

Authors
  1. G Treccani
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  2. L Musazzi
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  3. C Perego
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  4. M Milanese
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  5. N Nava
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  6. T Bonifacino
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  7. J Lamanna
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  8. A Malgaroli
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  9. F Drago
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  10. G Racagni
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  11. J R Nyengaard
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  12. G Wegener
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  13. G Bonanno
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  14. M Popoli
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Treccani, G., Musazzi, L., Perego, C. et al. Acute stress rapidly increases the readily releasable pool of glutamate vesicles in prefrontal and frontal cortex through non-genomic action of corticosterone. Mol Psychiatry 19, 401 (2014). https://doi.org/10.1038/mp.2014.20

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