---
_id: '8674'
abstract:
- lang: eng
text: '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.'
acknowledgement: We thank J. Angibaud for organotypic cultures and R. Chereau and
J. Tonnesen for help with the STED microscope; also D. Gonzales and the Neurocentre
Magendie INSERM U1215 Genotyping Platform, for breeding management and genotyping.
This work was supported by the Wellcome Trust Principal Fellowships 101896 and 212251,
ERC Advanced Grant 323113, ERC Proof-of-Concept Grant 767372, EC FP7 ITN 606950,
and EU CSA 811011 (D.A.R.); NRW-Rückkehrerpogramm, UCL Excellence Fellowship, German
Research Foundation (DFG) SPP1757 and SFB1089 (C.H.); Human Frontiers Science Program
(C.H., C.J.J., and H.J.); EMBO Long-Term Fellowship (L.B.); Marie Curie FP7 PIRG08-GA-2010-276995
(A.P.), ASTROMODULATION (S.R.); Equipe FRM DEQ 201 303 26519, Conseil Régional d’Aquitaine
R12056GG, INSERM (S.H.R.O.); ANR SUPERTri, ANR Castro (ANR-17-CE16-0002), R-13-BSV4-0007-01,
Université de Bordeaux, labex BRAIN (S.H.R.O. and U.V.N.); CNRS (A.P., S.H.R.O.,
and U.V.N.); HFSP, ANR CEXC, and France-BioImaging ANR-10-INSB-04 (U.V.N.); and
FP7 MemStick Project No. 201600 (M.G.S.).
article_processing_charge: No
article_type: original
author:
- first_name: Christian
full_name: Henneberger, Christian
last_name: Henneberger
- first_name: Lucie
full_name: Bard, Lucie
last_name: Bard
- first_name: Aude
full_name: Panatier, Aude
last_name: Panatier
- first_name: James P.
full_name: Reynolds, James P.
last_name: Reynolds
- first_name: Olga
full_name: Kopach, Olga
last_name: Kopach
- first_name: Nikolay I.
full_name: Medvedev, Nikolay I.
last_name: Medvedev
- first_name: Daniel
full_name: Minge, Daniel
last_name: Minge
- first_name: Michel K.
full_name: Herde, Michel K.
last_name: Herde
- first_name: Stefanie
full_name: Anders, Stefanie
last_name: Anders
- first_name: Igor
full_name: Kraev, Igor
last_name: Kraev
- first_name: Janosch P.
full_name: Heller, Janosch P.
last_name: Heller
- first_name: Sylvain
full_name: Rama, Sylvain
last_name: Rama
- first_name: Kaiyu
full_name: Zheng, Kaiyu
last_name: Zheng
- first_name: Thomas P.
full_name: Jensen, Thomas P.
last_name: Jensen
- first_name: Inmaculada
full_name: Sanchez-Romero, Inmaculada
id: 3D9C5D30-F248-11E8-B48F-1D18A9856A87
last_name: Sanchez-Romero
- first_name: Colin J.
full_name: Jackson, Colin J.
last_name: Jackson
- first_name: Harald L
full_name: Janovjak, Harald L
id: 33BA6C30-F248-11E8-B48F-1D18A9856A87
last_name: Janovjak
orcid: 0000-0002-8023-9315
- first_name: Ole Petter
full_name: Ottersen, Ole Petter
last_name: Ottersen
- first_name: Erlend Arnulf
full_name: Nagelhus, Erlend Arnulf
last_name: Nagelhus
- first_name: Stephane H.R.
full_name: Oliet, Stephane H.R.
last_name: Oliet
- first_name: Michael G.
full_name: Stewart, Michael G.
last_name: Stewart
- first_name: U. VAlentin
full_name: Nägerl, U. VAlentin
last_name: Nägerl
- first_name: 'Dmitri A. '
full_name: 'Rusakov, Dmitri A. '
last_name: Rusakov
citation:
ama: Henneberger C, Bard L, Panatier A, et al. LTP induction boosts glutamate spillover
by driving withdrawal of perisynaptic astroglia. Neuron. 2020;108(5):P919-936.E11.
doi:10.1016/j.neuron.2020.08.030
apa: Henneberger, C., Bard, L., Panatier, A., Reynolds, J. P., Kopach, O., Medvedev,
N. I., … Rusakov, D. A. (2020). LTP induction boosts glutamate spillover by driving
withdrawal of perisynaptic astroglia. Neuron. Elsevier. https://doi.org/10.1016/j.neuron.2020.08.030
chicago: Henneberger, Christian, Lucie Bard, Aude Panatier, James P. Reynolds, Olga
Kopach, Nikolay I. Medvedev, Daniel Minge, et al. “LTP Induction Boosts Glutamate
Spillover by Driving Withdrawal of Perisynaptic Astroglia.” Neuron. Elsevier,
2020. https://doi.org/10.1016/j.neuron.2020.08.030.
ieee: C. Henneberger et al., “LTP induction boosts glutamate spillover by
driving withdrawal of perisynaptic astroglia,” Neuron, vol. 108, no. 5.
Elsevier, p. P919–936.E11, 2020.
ista: Henneberger C, Bard L, Panatier A, Reynolds JP, Kopach O, Medvedev NI, Minge
D, Herde MK, Anders S, Kraev I, Heller JP, Rama S, Zheng K, Jensen TP, Sanchez-Romero
I, Jackson CJ, Janovjak HL, Ottersen OP, Nagelhus EA, Oliet SHR, Stewart MG, Nägerl
UVa, Rusakov DA. 2020. LTP induction boosts glutamate spillover by driving withdrawal
of perisynaptic astroglia. Neuron. 108(5), P919–936.E11.
mla: Henneberger, Christian, et al. “LTP Induction Boosts Glutamate Spillover by
Driving Withdrawal of Perisynaptic Astroglia.” Neuron, vol. 108, no. 5,
Elsevier, 2020, p. P919–936.E11, doi:10.1016/j.neuron.2020.08.030.
short: C. Henneberger, L. Bard, A. Panatier, J.P. Reynolds, O. Kopach, N.I. Medvedev,
D. Minge, M.K. Herde, S. Anders, I. Kraev, J.P. Heller, S. Rama, K. Zheng, T.P.
Jensen, I. Sanchez-Romero, C.J. Jackson, H.L. Janovjak, O.P. Ottersen, E.A. Nagelhus,
S.H.R. Oliet, M.G. Stewart, U.Va. Nägerl, D.A. Rusakov, Neuron 108 (2020) P919–936.E11.
date_created: 2020-10-18T22:01:38Z
date_published: 2020-12-09T00:00:00Z
date_updated: 2023-08-22T09:59:29Z
day: '09'
ddc:
- '570'
department:
- _id: HaJa
doi: 10.1016/j.neuron.2020.08.030
external_id:
isi:
- '000603428000010'
pmid:
- '32976770'
file:
- access_level: open_access
checksum: 054562bb50165ef9a1f46631c1c5e36b
content_type: application/pdf
creator: dernst
date_created: 2020-12-10T14:42:09Z
date_updated: 2020-12-10T14:42:09Z
file_id: '8939'
file_name: 2020_Neuron_Henneberger.pdf
file_size: 7518960
relation: main_file
success: 1
file_date_updated: 2020-12-10T14:42:09Z
has_accepted_license: '1'
intvolume: ' 108'
isi: 1
issue: '5'
language:
- iso: eng
license: https://creativecommons.org/licenses/by/4.0/
month: '12'
oa: 1
oa_version: Published Version
page: P919-936.E11
pmid: 1
publication: Neuron
publication_identifier:
eissn:
- '10974199'
issn:
- '08966273'
publication_status: published
publisher: Elsevier
quality_controlled: '1'
scopus_import: '1'
status: public
title: LTP induction boosts glutamate spillover by driving withdrawal of perisynaptic
astroglia
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 108
year: '2020'
...
---
_id: '7684'
article_processing_charge: No
article_type: original
author:
- first_name: Igor
full_name: Gridchyn, Igor
id: 4B60654C-F248-11E8-B48F-1D18A9856A87
last_name: Gridchyn
orcid: 0000-0002-1807-1929
- first_name: Philipp
full_name: Schönenberger, Philipp
id: 3B9D816C-F248-11E8-B48F-1D18A9856A87
last_name: Schönenberger
- first_name: Joseph
full_name: O'Neill, Joseph
id: 426376DC-F248-11E8-B48F-1D18A9856A87
last_name: O'Neill
- first_name: Jozsef L
full_name: Csicsvari, Jozsef L
id: 3FA14672-F248-11E8-B48F-1D18A9856A87
last_name: Csicsvari
orcid: 0000-0002-5193-4036
citation:
ama: Gridchyn I, Schönenberger P, O’Neill J, Csicsvari JL. Assembly-specific disruption
of hippocampal replay leads to selective memory deficit. Neuron. 2020;106(2):291-300.e6.
doi:10.1016/j.neuron.2020.01.021
apa: Gridchyn, I., Schönenberger, P., O’Neill, J., & Csicsvari, J. L. (2020).
Assembly-specific disruption of hippocampal replay leads to selective memory deficit.
Neuron. Elsevier. https://doi.org/10.1016/j.neuron.2020.01.021
chicago: Gridchyn, Igor, Philipp Schönenberger, Joseph O’Neill, and Jozsef L Csicsvari.
“Assembly-Specific Disruption of Hippocampal Replay Leads to Selective Memory
Deficit.” Neuron. Elsevier, 2020. https://doi.org/10.1016/j.neuron.2020.01.021.
ieee: I. Gridchyn, P. Schönenberger, J. O’Neill, and J. L. Csicsvari, “Assembly-specific
disruption of hippocampal replay leads to selective memory deficit,” Neuron,
vol. 106, no. 2. Elsevier, p. 291–300.e6, 2020.
ista: Gridchyn I, Schönenberger P, O’Neill J, Csicsvari JL. 2020. Assembly-specific
disruption of hippocampal replay leads to selective memory deficit. Neuron. 106(2),
291–300.e6.
mla: Gridchyn, Igor, et al. “Assembly-Specific Disruption of Hippocampal Replay
Leads to Selective Memory Deficit.” Neuron, vol. 106, no. 2, Elsevier,
2020, p. 291–300.e6, doi:10.1016/j.neuron.2020.01.021.
short: I. Gridchyn, P. Schönenberger, J. O’Neill, J.L. Csicsvari, Neuron 106 (2020)
291–300.e6.
date_created: 2020-04-26T22:00:45Z
date_published: 2020-04-22T00:00:00Z
date_updated: 2023-08-21T06:15:31Z
day: '22'
department:
- _id: JoCs
doi: 10.1016/j.neuron.2020.01.021
ec_funded: 1
external_id:
isi:
- '000528268200013'
pmid:
- '32070475'
intvolume: ' 106'
isi: 1
issue: '2'
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://doi.org/10.1016/j.neuron.2020.01.021
month: '04'
oa: 1
oa_version: Published Version
page: 291-300.e6
pmid: 1
project:
- _id: 257A4776-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '281511'
name: Memory-related information processing in neuronal circuits of the hippocampus
and entorhinal cortex
publication: Neuron
publication_identifier:
eissn:
- '10974199'
issn:
- '08966273'
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
link:
- description: News on IST Homepage
relation: press_release
url: https://ist.ac.at/en/news/librarian-of-memory/
scopus_import: '1'
status: public
title: Assembly-specific disruption of hippocampal replay leads to selective memory
deficit
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 106
year: '2020'
...
---
_id: '8001'
abstract:
- lang: eng
text: Post-tetanic potentiation (PTP) is an attractive candidate mechanism for hippocampus-dependent
short-term memory. Although PTP has a uniquely large magnitude at hippocampal
mossy fiber-CA3 pyramidal neuron synapses, it is unclear whether it can be induced
by natural activity and whether its lifetime is sufficient to support short-term
memory. We combined in vivo recordings from granule cells (GCs), in vitro paired
recordings from mossy fiber terminals and postsynaptic CA3 neurons, and “flash
and freeze” electron microscopy. PTP was induced at single synapses and showed
a low induction threshold adapted to sparse GC activity in vivo. PTP was mainly
generated by enlargement of the readily releasable pool of synaptic vesicles,
allowing multiplicative interaction with other plasticity forms. PTP was associated
with an increase in the docked vesicle pool, suggesting formation of structural
“pool engrams.” Absence of presynaptic activity extended the lifetime of the potentiation,
enabling prolonged information storage in the hippocampal network.
acknowledged_ssus:
- _id: SSU
acknowledgement: This project received funding from the European Research Council
(ERC) under the European Union Horizon 2020 Research and Innovation Program (grant
agreement 692692 to P.J.) and the Fond zur Förderung der Wissenschaftlichen Forschung
( Z 312-B27 , Wittgenstein award to P.J. and V 739-B27 to C.B.-M.). We thank Drs.
Jozsef Csicsvari, Jose Guzman, Erwin Neher, and Ryuichi Shigemoto for commenting
on earlier versions of the manuscript. We are grateful to Walter Kaufmann, Daniel
Gütl, and Vanessa Zheden for EM training; Alois Schlögl for programming; Florian
Marr for excellent technical assistance and cell reconstruction; Christina Altmutter
for technical help; Eleftheria Kralli-Beller for manuscript editing; Taija Makinen
for providing the Prox1-CreERT2 mouse line; and the Scientific Service Units of
IST Austria for support.
article_processing_charge: No
article_type: original
author:
- first_name: David H
full_name: Vandael, David H
id: 3AE48E0A-F248-11E8-B48F-1D18A9856A87
last_name: Vandael
orcid: 0000-0001-7577-1676
- first_name: Carolina
full_name: Borges Merjane, Carolina
id: 4305C450-F248-11E8-B48F-1D18A9856A87
last_name: Borges Merjane
orcid: 0000-0003-0005-401X
- first_name: Xiaomin
full_name: Zhang, Xiaomin
id: 423EC9C2-F248-11E8-B48F-1D18A9856A87
last_name: Zhang
- first_name: Peter M
full_name: Jonas, Peter M
id: 353C1B58-F248-11E8-B48F-1D18A9856A87
last_name: Jonas
orcid: 0000-0001-5001-4804
citation:
ama: Vandael DH, Borges Merjane C, Zhang X, Jonas PM. Short-term plasticity at hippocampal
mossy fiber synapses is induced by natural activity patterns and associated with
vesicle pool engram formation. Neuron. 2020;107(3):509-521. doi:10.1016/j.neuron.2020.05.013
apa: Vandael, D. H., Borges Merjane, C., Zhang, X., & Jonas, P. M. (2020). Short-term
plasticity at hippocampal mossy fiber synapses is induced by natural activity
patterns and associated with vesicle pool engram formation. Neuron. Elsevier.
https://doi.org/10.1016/j.neuron.2020.05.013
chicago: Vandael, David H, Carolina Borges Merjane, Xiaomin Zhang, and Peter M Jonas.
“Short-Term Plasticity at Hippocampal Mossy Fiber Synapses Is Induced by Natural
Activity Patterns and Associated with Vesicle Pool Engram Formation.” Neuron.
Elsevier, 2020. https://doi.org/10.1016/j.neuron.2020.05.013.
ieee: D. H. Vandael, C. Borges Merjane, X. Zhang, and P. M. Jonas, “Short-term plasticity
at hippocampal mossy fiber synapses is induced by natural activity patterns and
associated with vesicle pool engram formation,” Neuron, vol. 107, no. 3.
Elsevier, pp. 509–521, 2020.
ista: Vandael DH, Borges Merjane C, Zhang X, Jonas PM. 2020. Short-term plasticity
at hippocampal mossy fiber synapses is induced by natural activity patterns and
associated with vesicle pool engram formation. Neuron. 107(3), 509–521.
mla: Vandael, David H., et al. “Short-Term Plasticity at Hippocampal Mossy Fiber
Synapses Is Induced by Natural Activity Patterns and Associated with Vesicle Pool
Engram Formation.” Neuron, vol. 107, no. 3, Elsevier, 2020, pp. 509–21,
doi:10.1016/j.neuron.2020.05.013.
short: D.H. Vandael, C. Borges Merjane, X. Zhang, P.M. Jonas, Neuron 107 (2020)
509–521.
date_created: 2020-06-22T13:29:05Z
date_published: 2020-08-05T00:00:00Z
date_updated: 2023-08-22T07:45:25Z
day: '05'
ddc:
- '570'
department:
- _id: PeJo
doi: 10.1016/j.neuron.2020.05.013
ec_funded: 1
external_id:
isi:
- '000556135600004'
pmid:
- '32492366'
file:
- access_level: open_access
checksum: 4030b2be0c9625d54694a1e9fb00305e
content_type: application/pdf
creator: dernst
date_created: 2020-11-25T11:23:02Z
date_updated: 2020-11-25T11:23:02Z
file_id: '8811'
file_name: 2020_Neuron_Vandael.pdf
file_size: 4390833
relation: main_file
success: 1
file_date_updated: 2020-11-25T11:23:02Z
has_accepted_license: '1'
intvolume: ' 107'
isi: 1
issue: '3'
language:
- iso: eng
license: https://creativecommons.org/licenses/by-nc-nd/4.0/
month: '08'
oa: 1
oa_version: Published Version
page: 509-521
pmid: 1
project:
- _id: 25B7EB9E-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '692692'
name: Biophysics and circuit function of a giant cortical glumatergic synapse
- _id: 25C5A090-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: Z00312
name: The Wittgenstein Prize
- _id: 2696E7FE-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: V00739
name: Structural plasticity at mossy fiber-CA3 synapses
publication: Neuron
publication_identifier:
eissn:
- '10974199'
issn:
- 0896-6273
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
link:
- description: News on IST Homepage
relation: press_release
url: https://ist.ac.at/en/news/possible-physical-trace-of-short-term-memory-found/
scopus_import: '1'
status: public
title: Short-term plasticity at hippocampal mossy fiber synapses is induced by natural
activity patterns and associated with vesicle pool engram formation
tmp:
image: /images/cc_by_nc_nd.png
legal_code_url: https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode
name: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
(CC BY-NC-ND 4.0)
short: CC BY-NC-ND (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 107
year: '2020'
...
---
_id: '6830'
article_processing_charge: No
article_type: letter_note
author:
- first_name: Ximena
full_name: Contreras, Ximena
id: 475990FE-F248-11E8-B48F-1D18A9856A87
last_name: Contreras
- first_name: Simon
full_name: Hippenmeyer, Simon
id: 37B36620-F248-11E8-B48F-1D18A9856A87
last_name: Hippenmeyer
orcid: 0000-0003-2279-1061
citation:
ama: Contreras X, Hippenmeyer S. Memo1 tiles the radial glial cell grid. Neuron.
2019;103(5):750-752. doi:10.1016/j.neuron.2019.08.021
apa: Contreras, X., & Hippenmeyer, S. (2019). Memo1 tiles the radial glial cell
grid. Neuron. Elsevier. https://doi.org/10.1016/j.neuron.2019.08.021
chicago: Contreras, Ximena, and Simon Hippenmeyer. “Memo1 Tiles the Radial Glial
Cell Grid.” Neuron. Elsevier, 2019. https://doi.org/10.1016/j.neuron.2019.08.021.
ieee: X. Contreras and S. Hippenmeyer, “Memo1 tiles the radial glial cell grid,”
Neuron, vol. 103, no. 5. Elsevier, pp. 750–752, 2019.
ista: Contreras X, Hippenmeyer S. 2019. Memo1 tiles the radial glial cell grid.
Neuron. 103(5), 750–752.
mla: Contreras, Ximena, and Simon Hippenmeyer. “Memo1 Tiles the Radial Glial Cell
Grid.” Neuron, vol. 103, no. 5, Elsevier, 2019, pp. 750–52, doi:10.1016/j.neuron.2019.08.021.
short: X. Contreras, S. Hippenmeyer, Neuron 103 (2019) 750–752.
date_created: 2019-08-25T22:00:50Z
date_published: 2019-09-04T00:00:00Z
date_updated: 2024-03-25T23:30:23Z
day: '04'
department:
- _id: SiHi
doi: 10.1016/j.neuron.2019.08.021
external_id:
isi:
- '000484400200002'
pmid:
- '31487522'
intvolume: ' 103'
isi: 1
issue: '5'
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://doi.org/10.1016/j.neuron.2019.08.021
month: '09'
oa: 1
oa_version: Published Version
page: 750-752
pmid: 1
publication: Neuron
publication_identifier:
eissn:
- '10974199'
issn:
- '08966273'
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
record:
- id: '7902'
relation: part_of_dissertation
status: public
scopus_import: '1'
status: public
title: Memo1 tiles the radial glial cell grid
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 103
year: '2019'
...