Journal Article

DZNE-2022-00941

http://join2-wiki.gsi.de/foswiki/pub/Main/Artwork/join2_logo100x88.png LTP Induction Boosts Glutamate Spillover by Driving Withdrawal of Perisynaptic Astroglia.

Henneberger, C. (First author)DZNE* ; Bard, L. ; Panatier, A. ; Reynolds, J. P. ; Kopach, O. ; Medvedev, N. I. ; Minge, D. ; Herde, M. K. ; Anders, S. ; Kraev, I. ; Heller, J. P. ; Rama, S. ; Zheng, K. ; Jensen, T. P. ; Sanchez-Romero, I. ; Jackson, C. J. ; Janovjak, H. ; Ottersen, O. P. ; Nagelhus, E. A. ; Oliet, S. H. R. ; Stewart, M. G. ; Nägerl, U. V. ; Rusakov, D. A.

2020
Elsevier New York, NY

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Please use a persistent id in citations: doi:10.1016/j.neuron.2020.08.030

Abstract: Extrasynaptic actions of glutamate are limited by high-affinity transporters expressed by perisynaptic astroglial processes (PAPs): this helps maintain point-to-point transmission in excitatory circuits. Memory formation in the brain is associated with synaptic remodeling, but how this affects PAPs and therefore extrasynaptic glutamate actions is poorly understood. Here, we used advanced imaging methods, in situ and in vivo, to find that a classical synaptic memory mechanism, long-term potentiation (LTP), triggers withdrawal of PAPs from potentiated synapses. Optical glutamate sensors combined with patch-clamp and 3D molecular localization reveal that LTP induction thus prompts spatial retreat of astroglial glutamate transporters, boosting glutamate spillover and NMDA-receptor-mediated inter-synaptic cross-talk. The LTP-triggered PAP withdrawal involves NKCC1 transporters and the actin-controlling protein cofilin but does not depend on major Ca2+-dependent cascades in astrocytes. We have therefore uncovered a mechanism by which a memory trace at one synapse could alter signal handling by multiple neighboring connections.

Keyword(s): Animals (MeSH) ; Astrocytes: metabolism (MeSH) ; Astrocytes: ultrastructure (MeSH) ; Female (MeSH) ; Glutamic Acid: metabolism (MeSH) ; Imaging, Three-Dimensional: methods (MeSH) ; Long-Term Potentiation: physiology (MeSH) ; Male (MeSH) ; Mice (MeSH) ; Mice, Inbred C57BL (MeSH) ; Mice, Knockout (MeSH) ; Mice, Transgenic (MeSH) ; Organ Culture Techniques (MeSH) ; Rats (MeSH) ; Rats, Sprague-Dawley (MeSH) ; Rats, Wistar (MeSH) ; Synapses: metabolism (MeSH) ; Synapses: ultrastructure (MeSH) ; Excitatory synapse ; astrocyte plasticity ; barrel cortex ; glutamate sensor imaging ; glutamate spillover ; hippocampus ; long-term potentiation ; perisynaptic astroglial processes ; super-resolution microscopy ; whisker stimulation ; Glutamic Acid

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Contributing Institute(s):

1. Synaptic and Glial Plasticity (AG Henneberger)

Research Program(s):

1. 899 - ohne Topic (POF4-899) (POF4-899)

Appears in the scientific report 2020

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Database coverage:
; ; ; BIOSIS Previews ; Biological Abstracts ; Clarivate Analytics Master Journal List ; Current Contents - Life Sciences ; Ebsco Academic Search ; Essential Science Indicators ; IF >= 15 ; JCR ; Nationallizenz ; SCOPUS ; Science Citation Index Expanded ; Web of Science Core Collection

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