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LTP Induction Boosts Glutamate Spillover by Driving Withdrawal of Perisynaptic Astroglia

Henneberger, Christian ; Bard, Lucie ; Panatier, Aude ; Reynolds, James P. ; Kopach, Olga ; Medvedev, Nikolay I. ; Minge, Daniel ; Herde, Michel K. ; Anders, Stefanie ; Kraev, Igor ; Heller, Janosch P. ; Rama, Sylvain ; Zheng, Kaiyu ; Jensen, Thomas P. ; Sanchez-Romero, Inmaculada ; Jackson, Colin J. ; Janovjak, Harald ; Ottersen, Ole Petter ; Nagelhus, Erlend Arnulf ; Oliet, Stephane H.R. ; Stewart, Michael G. ; Nägerl, U. Valentin ; Rusakov, Dmitri A.

Neuron (Cambridge, Mass.), 2020-12, Vol.108 (5), p.919-936.e11 [Periódico revisado por pares]

United States: Elsevier Inc

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Título:
LTP Induction Boosts Glutamate Spillover by Driving Withdrawal of Perisynaptic Astroglia
Autor: Henneberger, Christian ; Bard, Lucie ; Panatier, Aude ; Reynolds, James P. ; Kopach, Olga ; Medvedev, Nikolay I. ; Minge, Daniel ; Herde, Michel K. ; Anders, Stefanie ; Kraev, Igor ; Heller, Janosch P. ; Rama, Sylvain ; Zheng, Kaiyu ; Jensen, Thomas P. ; Sanchez-Romero, Inmaculada ; Jackson, Colin J. ; Janovjak, Harald ; Ottersen, Ole Petter ; Nagelhus, Erlend Arnulf ; Oliet, Stephane H.R. ; Stewart, Michael G. ; Nägerl, U. Valentin ; Rusakov, Dmitri A.
Assuntos: Actin ; Animals ; astrocyte plasticity ; Astrocytes ; Astrocytes - metabolism ; Astrocytes - ultrastructure ; barrel cortex ; Calcium ; Chloride transport ; Cofilin ; Excitatory synapse ; Female ; glutamate sensor imaging ; glutamate spillover ; Glutamic Acid - metabolism ; Glutamic acid receptors (ionotropic) ; hippocampus ; Imaging, Three-Dimensional - methods ; Life Sciences ; Localization ; Long-term potentiation ; Long-Term Potentiation - physiology ; Male ; Medicin och hälsovetenskap ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Mice, Transgenic ; Microscopy ; N-Methyl-D-aspartic acid receptors ; Neurobiology ; Neuroimaging ; Neurons and Cognition ; Organ Culture Techniques ; perisynaptic astroglial processes ; Rats ; Rats, Sprague-Dawley ; Rats, Wistar ; super-resolution microscopy ; Synapses - metabolism ; Synapses - ultrastructure ; whisker stimulation
É parte de: Neuron (Cambridge, Mass.), 2020-12, Vol.108 (5), p.919-936.e11
Notas: ObjectType-Article-1
SourceType-Scholarly Journals-1
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Lead Contact
Dr Nagelhus sadly passed away on 10 January 2020
These authors contributed equally
Descrição: 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. •Induction of synaptic LTP prompts withdrawal of perisynaptic astroglia•The underlying mechanisms involve NKCC1 transporter and cofilin•Reduced synaptic astroglial coverage boosts extrasynaptic glutamate escape•LTP induction thus enhances NMDAR-dependent inter-synaptic cross-talk Central synapses are often surrounded by thin astroglial processes that confine chemical neurotransmission to the synaptic cleft. Henneberger et al. find that memory trace formation at synaptic connections prompts withdrawal of these processes, thus boosting extrasynaptic neurotransmitter actions. Such actions can alter signal integration rules among neighboring synapses.
Editor: United States: Elsevier Inc
Idioma: Inglês;Norueguês

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LTP Induction Boosts Glutamate Spillover by Driving Withdrawal of Perisynaptic Astroglia

United States: Elsevier Inc

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