---
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abstract:
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text: The coupling between Ca2+ channels and release sensors is a key factor defining
the signaling properties of a synapse. However, the coupling nanotopography at
many synapses remains unknown, and it is unclear how it changes during development.
To address these questions, we examined coupling at the cerebellar inhibitory
basket cell (BC)-Purkinje cell (PC) synapse. Biophysical analysis of transmission
by paired recording and intracellular pipette perfusion revealed that the effects
of exogenous Ca2+ chelators decreased during development, despite constant reliance
of release on P/Q-type Ca2+ channels. Structural analysis by freeze-fracture replica
labeling (FRL) and transmission electron microscopy (EM) indicated that presynaptic
P/Q-type Ca2+ channels formed nanoclusters throughout development, whereas docked
vesicles were only clustered at later developmental stages. Modeling suggested
a developmental transformation from a more random to a more clustered coupling
nanotopography. Thus, presynaptic signaling developmentally approaches a point-to-point
configuration, optimizing speed, reliability, and energy efficiency of synaptic
transmission.
acknowledged_ssus:
- _id: EM-Fac
- _id: PreCl
- _id: M-Shop
acknowledgement: We thank Drs. David DiGregorio and Erwin Neher for critically reading
an earlier version of the manuscript, Ralf Schneggenburger for helpful discussions,
Benjamin Suter and Katharina Lichter for support with image analysis, Chris Wojtan
for advice on numerical solution of partial differential equations, Maria Reva for
help with Ripley analysis, Alois Schlögl for programming, and Akari Hagiwara and
Toshihisa Ohtsuka for anti-ELKS antibody. We are grateful to Florian Marr, Christina
Altmutter, and Vanessa Zheden for excellent technical assistance and to Eleftheria
Kralli-Beller for manuscript editing. This research was supported by the Scientific
Services Units (SSUs) of ISTA (Electron Microscopy Facility, Preclinical Facility,
and Machine Shop). The project received funding from the European Research Council
(ERC) under the European Union’s Horizon 2020 research and innovation program (grant
agreement no. 692692), the Fonds zur Förderung der Wissenschaftlichen Forschung
(Z 312-B27, Wittgenstein award; P 36232-B), all to P.J., and a DOC fellowship of
the Austrian Academy of Sciences to J.-J.C.
article_processing_charge: Yes (via OA deal)
article_type: original
author:
- first_name: JingJing
full_name: Chen, JingJing
id: 2C4E65C8-F248-11E8-B48F-1D18A9856A87
last_name: Chen
- first_name: Walter
full_name: Kaufmann, Walter
id: 3F99E422-F248-11E8-B48F-1D18A9856A87
last_name: Kaufmann
orcid: 0000-0001-9735-5315
- first_name: Chong
full_name: Chen, Chong
id: 3DFD581A-F248-11E8-B48F-1D18A9856A87
last_name: Chen
- first_name: Itaru
full_name: Arai, Itaru
id: 32A73F6C-F248-11E8-B48F-1D18A9856A87
last_name: Arai
- first_name: Olena
full_name: Kim, Olena
id: 3F8ABDDA-F248-11E8-B48F-1D18A9856A87
last_name: Kim
orcid: 0000-0003-2344-1039
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- 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: Chen J, Kaufmann W, Chen C, et al. Developmental transformation of Ca2+ channel-vesicle
nanotopography at a central GABAergic synapse. Neuron. 2024;112(5):755-771.e9.
doi:10.1016/j.neuron.2023.12.002
apa: Chen, J., Kaufmann, W., Chen, C., Arai, itaru, Kim, O., Shigemoto, R., &
Jonas, P. M. (2024). Developmental transformation of Ca2+ channel-vesicle nanotopography
at a central GABAergic synapse. Neuron. Elsevier. https://doi.org/10.1016/j.neuron.2023.12.002
chicago: Chen, JingJing, Walter Kaufmann, Chong Chen, itaru Arai, Olena Kim, Ryuichi
Shigemoto, and Peter M Jonas. “Developmental Transformation of Ca2+ Channel-Vesicle
Nanotopography at a Central GABAergic Synapse.” Neuron. Elsevier, 2024.
https://doi.org/10.1016/j.neuron.2023.12.002.
ieee: J. Chen et al., “Developmental transformation of Ca2+ channel-vesicle
nanotopography at a central GABAergic synapse,” Neuron, vol. 112, no. 5.
Elsevier, p. 755–771.e9, 2024.
ista: Chen J, Kaufmann W, Chen C, Arai itaru, Kim O, Shigemoto R, Jonas PM. 2024.
Developmental transformation of Ca2+ channel-vesicle nanotopography at a central
GABAergic synapse. Neuron. 112(5), 755–771.e9.
mla: Chen, JingJing, et al. “Developmental Transformation of Ca2+ Channel-Vesicle
Nanotopography at a Central GABAergic Synapse.” Neuron, vol. 112, no. 5,
Elsevier, 2024, p. 755–771.e9, doi:10.1016/j.neuron.2023.12.002.
short: J. Chen, W. Kaufmann, C. Chen, itaru Arai, O. Kim, R. Shigemoto, P.M. Jonas,
Neuron 112 (2024) 755–771.e9.
corr_author: '1'
date_created: 2024-01-21T23:00:56Z
date_published: 2024-03-06T00:00:00Z
date_updated: 2026-04-28T22:30:24Z
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doi: 10.1016/j.neuron.2023.12.002
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external_id:
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name: Development of nanodomain coupling between Ca2+ channels and release sensors
at a central inhibitory synapse
publication: Neuron
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scopus_import: '1'
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title: Developmental transformation of Ca2+ channel-vesicle nanotopography at a central
GABAergic synapse
tmp:
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...
---
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abstract:
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text: Neuronal networks in the brain consist of two main types of neuron, glutamatergic
principal neurons and GABAergic interneurons. Although these interneurons only
represent 10–20% of the whole population, they mediate feedback and feedforward
inhibition and are involved in the generation of high-frequency network oscillations.
A hallmark functional property of GABAergic interneurons, especially of the parvalbumin‑expressing
(PV+) subtypes, is the speed of signaling at their output synapse across species
and brain regions. Several molecular and subcellular factors may underlie the
submillisecond signaling at GABAergic synapses. Such as the selective use of P/Q
type Ca2+ channels and the tight coupling between Ca2+ channels and Ca2+ sensors
of exocytosis. However, whether the molecular identity of the release sensor contributes
to these signaling properties remains unclear. Besides, these interneurons are
mainly show depression in response to train of stimuli. How could they keep sufficient
release to control the activity of postsynaptic principal neurons during high
network activity, is largely elusive. For my Ph.D. work, we firstly examined the
Ca2+ sensor of exocytosis at the GABAergic basket cell (BC) to Purkinje cell (PC)
synapse in the cerebellum. Immunolabeling suggested that BC terminals selectively
expressed synaptotagmin 2 (Syt2), whereas synaptotagmin 1 (Syt1) was enriched
in excitatory terminals. Genetic elimination of Syt2 reduced action potential-evoked
release to ~10% compared to the wild-type control, identifying Syt2 as the major
Ca2+ sensor at BC‑PC synapses. Differential adenovirus-mediated rescue revealed
Syt2 triggered release with shorter latency and higher temporal precision, and
mediated faster vesicle pool replenishment than Syt1. Furthermore, deletion of
Syt2 severely reduced and delayed disynaptic inhibition following parallel fiber
stimulation. Thus, the selective use of Syt2 as the release sensor at BC–PC synapse
ensures fast feedforward inhibition in cerebellar microcircuits. Additionally,
we tested the function of another synaptotagmin member, Syt7, for inhibitory synaptic
transmission at the BC–PC synapse. Syt7 is thought to be a Ca2+ sensor that mediates
asynchronous transmitter release and facilitation at synapses. However, it is
strongly expressed in fast-spiking, PV+ GABAergic interneurons and the output
synapses of these neurons produce only minimal asynchronous release and show depression
rather than facilitation. How could Syt7, a facilitation sensor, contribute to
the depressed inhibitory synaptic transmission needs to be further investigated
and understood. Our results indicated that at the BC–PC synapse, Syt7 contributes
to asynchronous release, pool replenishment and facilitation. In combination,
these three effects ensure efficient transmitter release during high‑frequency
activity and guarantee frequency independence of inhibition. Taken together, our
results confirmed that Syt2, which has the fastest kinetic properties among all
synaptotagmin members, is mainly used by the inhibitory BC‑PC synapse for synaptic
transmission, contributing to the speed and temporal precision of transmitter
release. Furthermore, we showed that Syt7, another highly expressed synaptotagmin
member in the output synapses of cerebellar BCs, is used for ensuring efficient
inhibitor synaptic transmission during high activity.
alternative_title:
- ISTA Thesis
article_processing_charge: No
author:
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full_name: Chen, Chong
id: 3DFD581A-F248-11E8-B48F-1D18A9856A87
last_name: Chen
citation:
ama: Chen C. Synaptotagmins ensure speed and efficiency of inhibitory neurotransmitter
release. 2018. doi:10.15479/AT:ISTA:th_997
apa: Chen, C. (2018). Synaptotagmins ensure speed and efficiency of inhibitory
neurotransmitter release. Institute of Science and Technology Austria. https://doi.org/10.15479/AT:ISTA:th_997
chicago: Chen, Chong. “Synaptotagmins Ensure Speed and Efficiency of Inhibitory
Neurotransmitter Release.” Institute of Science and Technology Austria, 2018.
https://doi.org/10.15479/AT:ISTA:th_997.
ieee: C. Chen, “Synaptotagmins ensure speed and efficiency of inhibitory neurotransmitter
release,” Institute of Science and Technology Austria, 2018.
ista: Chen C. 2018. Synaptotagmins ensure speed and efficiency of inhibitory neurotransmitter
release. Institute of Science and Technology Austria.
mla: Chen, Chong. Synaptotagmins Ensure Speed and Efficiency of Inhibitory Neurotransmitter
Release. Institute of Science and Technology Austria, 2018, doi:10.15479/AT:ISTA:th_997.
short: C. Chen, Synaptotagmins Ensure Speed and Efficiency of Inhibitory Neurotransmitter
Release, Institute of Science and Technology Austria, 2018.
corr_author: '1'
date_created: 2018-12-11T11:45:49Z
date_published: 2018-03-01T00:00:00Z
date_updated: 2026-04-08T14:09:29Z
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related_material:
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status: public
- id: '749'
relation: part_of_dissertation
status: public
status: public
supervisor:
- first_name: Peter M
full_name: Jonas, Peter M
id: 353C1B58-F248-11E8-B48F-1D18A9856A87
last_name: Jonas
orcid: 0000-0001-5001-4804
title: Synaptotagmins ensure speed and efficiency of inhibitory neurotransmitter release
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)
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type: dissertation
user_id: ba8df636-2132-11f1-aed0-ed93e2281fdd
year: '2018'
...
---
_id: '1117'
abstract:
- lang: eng
text: 'GABAergic synapses in brain circuits generate inhibitory output signals with
submillisecond latency and temporal precision. Whether the molecular identity
of the release sensor contributes to these signaling properties remains unclear.
Here, we examined the Ca^2+ sensor of exocytosis at GABAergic basket cell (BC)
to Purkinje cell (PC) synapses in cerebellum. Immunolabeling suggested that BC
terminals selectively expressed synaptotagmin 2 (Syt2), whereas synaptotagmin
1 (Syt1) was enriched in excitatory terminals. Genetic elimination of Syt2 reduced
action potential-evoked release to ∼10%, identifying Syt2 as the major Ca^2+ sensor
at BC-PC synapses. Differential adenovirus-mediated rescue revealed that Syt2
triggered release with shorter latency and higher temporal precision and mediated
faster vesicle pool replenishment than Syt1. Furthermore, deletion of Syt2 severely
reduced and delayed disynaptic inhibition following parallel fiber stimulation.
Thus, the selective use of Syt2 as release sensor at BC-PC synapses ensures fast
and efficient feedforward inhibition in cerebellar microcircuits. #bioimagingfacility-author'
acknowledged_ssus:
- _id: Bio
- _id: PreCl
article_processing_charge: No
author:
- first_name: Chong
full_name: Chen, Chong
id: 3DFD581A-F248-11E8-B48F-1D18A9856A87
last_name: Chen
- first_name: Itaru
full_name: Arai, Itaru
id: 32A73F6C-F248-11E8-B48F-1D18A9856A87
last_name: Arai
- first_name: Rachel
full_name: Satterield, Rachel
last_name: Satterield
- first_name: Samuel
full_name: Young, Samuel
last_name: Young
- 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: Chen C, Arai itaru, Satterield R, Young S, Jonas PM. Synaptotagmin 2 is the
fast Ca2+ sensor at a central inhibitory synapse. Cell Reports. 2017;18(3):723-736.
doi:10.1016/j.celrep.2016.12.067
apa: Chen, C., Arai, itaru, Satterield, R., Young, S., & Jonas, P. M. (2017).
Synaptotagmin 2 is the fast Ca2+ sensor at a central inhibitory synapse. Cell
Reports. Cell Press. https://doi.org/10.1016/j.celrep.2016.12.067
chicago: Chen, Chong, itaru Arai, Rachel Satterield, Samuel Young, and Peter M Jonas.
“Synaptotagmin 2 Is the Fast Ca2+ Sensor at a Central Inhibitory Synapse.” Cell
Reports. Cell Press, 2017. https://doi.org/10.1016/j.celrep.2016.12.067.
ieee: C. Chen, itaru Arai, R. Satterield, S. Young, and P. M. Jonas, “Synaptotagmin
2 is the fast Ca2+ sensor at a central inhibitory synapse,” Cell Reports,
vol. 18, no. 3. Cell Press, pp. 723–736, 2017.
ista: Chen C, Arai itaru, Satterield R, Young S, Jonas PM. 2017. Synaptotagmin
2 is the fast Ca2+ sensor at a central inhibitory synapse. Cell Reports. 18(3),
723–736.
mla: Chen, Chong, et al. “Synaptotagmin 2 Is the Fast Ca2+ Sensor at a Central Inhibitory
Synapse.” Cell Reports, vol. 18, no. 3, Cell Press, 2017, pp. 723–36, doi:10.1016/j.celrep.2016.12.067.
short: C. Chen, itaru Arai, R. Satterield, S. Young, P.M. Jonas, Cell Reports 18
(2017) 723–736.
date_created: 2018-12-11T11:50:14Z
date_published: 2017-01-17T00:00:00Z
date_updated: 2026-04-08T14:09:28Z
day: '17'
ddc:
- '571'
department:
- _id: PeJo
doi: 10.1016/j.celrep.2016.12.067
ec_funded: 1
external_id:
isi:
- '000396470600013'
file:
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call_identifier: FWF
grant_number: P24909-B24
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- _id: 25C0F108-B435-11E9-9278-68D0E5697425
call_identifier: FP7
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name: Nanophysiology of fast-spiking, parvalbumin-expressing GABAergic interneurons
publication: Cell Reports
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title: Synaptotagmin 2 is the fast Ca2+ sensor at a central inhibitory synapse
tmp:
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name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
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type: journal_article
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year: '2017'
...
---
_id: '749'
abstract:
- lang: eng
text: 'Synaptotagmin 7 (Syt7) is thought to be a Ca2+ sensor that mediates asynchronous
transmitter release and facilitation at synapses. However, Syt7 is strongly expressed
in fast-spiking, parvalbumin-expressing GABAergic interneurons, and the output
synapses of these neurons produce only minimal asynchronous release and show depression
rather than facilitation. To resolve this apparent contradiction, we examined
the effects of genetic elimination of Syt7 on synaptic transmission at the GABAergic
basket cell (BC)-Purkinje cell (PC) synapse in cerebellum. Our results indicate
that at the BC-PC synapse, Syt7 contributes to asynchronous release, pool replenishment,
and facilitation. In combination, these three effects ensure efficient transmitter
release during high-frequency activity and guarantee frequency independence of
inhibition. Our results identify a distinct function of Syt7: ensuring the efficiency
of high-frequency inhibitory synaptic transmission'
acknowledged_ssus:
- _id: PreCl
article_processing_charge: No
author:
- first_name: Chong
full_name: Chen, Chong
id: 3DFD581A-F248-11E8-B48F-1D18A9856A87
last_name: Chen
- first_name: Rachel
full_name: Satterfield, Rachel
last_name: Satterfield
- first_name: Samuel
full_name: Young, Samuel
last_name: Young
- 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: Chen C, Satterfield R, Young S, Jonas PM. Triple function of Synaptotagmin
7 ensures efficiency of high-frequency transmission at central GABAergic synapses.
Cell Reports. 2017;21(8):2082-2089. doi:10.1016/j.celrep.2017.10.122
apa: Chen, C., Satterfield, R., Young, S., & Jonas, P. M. (2017). Triple function
of Synaptotagmin 7 ensures efficiency of high-frequency transmission at central
GABAergic synapses. Cell Reports. Cell Press. https://doi.org/10.1016/j.celrep.2017.10.122
chicago: Chen, Chong, Rachel Satterfield, Samuel Young, and Peter M Jonas. “Triple
Function of Synaptotagmin 7 Ensures Efficiency of High-Frequency Transmission
at Central GABAergic Synapses.” Cell Reports. Cell Press, 2017. https://doi.org/10.1016/j.celrep.2017.10.122.
ieee: C. Chen, R. Satterfield, S. Young, and P. M. Jonas, “Triple function of Synaptotagmin
7 ensures efficiency of high-frequency transmission at central GABAergic synapses,”
Cell Reports, vol. 21, no. 8. Cell Press, pp. 2082–2089, 2017.
ista: Chen C, Satterfield R, Young S, Jonas PM. 2017. Triple function of Synaptotagmin
7 ensures efficiency of high-frequency transmission at central GABAergic synapses.
Cell Reports. 21(8), 2082–2089.
mla: Chen, Chong, et al. “Triple Function of Synaptotagmin 7 Ensures Efficiency
of High-Frequency Transmission at Central GABAergic Synapses.” Cell Reports,
vol. 21, no. 8, Cell Press, 2017, pp. 2082–89, doi:10.1016/j.celrep.2017.10.122.
short: C. Chen, R. Satterfield, S. Young, P.M. Jonas, Cell Reports 21 (2017) 2082–2089.
corr_author: '1'
date_created: 2018-12-11T11:48:18Z
date_published: 2017-11-21T00:00:00Z
date_updated: 2026-04-08T14:09:28Z
day: '21'
ddc:
- '570'
- '571'
department:
- _id: PeJo
doi: 10.1016/j.celrep.2017.10.122
ec_funded: 1
external_id:
isi:
- '000416216700007'
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grant_number: P24909-B24
name: Mechanisms of transmitter release at GABAergic synapses
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call_identifier: H2020
grant_number: '692692'
name: Biophysics and circuit function of a giant cortical glutamatergic synapse
publication: Cell Reports
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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: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 21
year: '2017'
...
---
_id: '991'
abstract:
- lang: eng
text: Synaptotagmin 7 (Syt7) was originally identified as a slow Ca2+ sensor for
lysosome fusion, but its function at fast synapses is controversial. The paper
by Luo and Südhof (2017) in this issue of Neuron shows that at the calyx of Held
in the auditory brainstem Syt7 triggers asynchronous release during stimulus trains,
resulting in reliable and temporally precise high-frequency transmission. Thus,
a slow Ca2+ sensor contributes to the fast signaling properties of the calyx synapse.
article_processing_charge: No
author:
- first_name: Chong
full_name: Chen, Chong
id: 3DFD581A-F248-11E8-B48F-1D18A9856A87
last_name: Chen
- 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: 'Chen C, Jonas PM. Synaptotagmins: That’s why so many. Neuron. 2017;94(4):694-696.
doi:10.1016/j.neuron.2017.05.011'
apa: 'Chen, C., & Jonas, P. M. (2017). Synaptotagmins: That’s why so many. Neuron.
Elsevier. https://doi.org/10.1016/j.neuron.2017.05.011'
chicago: 'Chen, Chong, and Peter M Jonas. “Synaptotagmins: That’s Why so Many.”
Neuron. Elsevier, 2017. https://doi.org/10.1016/j.neuron.2017.05.011.'
ieee: 'C. Chen and P. M. Jonas, “Synaptotagmins: That’s why so many,” Neuron,
vol. 94, no. 4. Elsevier, pp. 694–696, 2017.'
ista: 'Chen C, Jonas PM. 2017. Synaptotagmins: That’s why so many. Neuron. 94(4),
694–696.'
mla: 'Chen, Chong, and Peter M. Jonas. “Synaptotagmins: That’s Why so Many.” Neuron,
vol. 94, no. 4, Elsevier, 2017, pp. 694–96, doi:10.1016/j.neuron.2017.05.011.'
short: C. Chen, P.M. Jonas, Neuron 94 (2017) 694–696.
date_created: 2018-12-11T11:49:34Z
date_published: 2017-05-17T00:00:00Z
date_updated: 2026-04-16T10:05:51Z
day: '17'
department:
- _id: PeJo
doi: 10.1016/j.neuron.2017.05.011
external_id:
isi:
- '000401415100002'
intvolume: ' 94'
isi: 1
issue: '4'
language:
- iso: eng
month: '05'
oa_version: None
page: 694 - 696
publication: Neuron
publication_identifier:
issn:
- 0896-6273
publication_status: published
publisher: Elsevier
publist_id: '6408'
quality_controlled: '1'
scopus_import: '1'
status: public
title: 'Synaptotagmins: That’s why so many'
type: journal_article
user_id: ba8df636-2132-11f1-aed0-ed93e2281fdd
volume: 94
year: '2017'
...
---
_id: '1834'
abstract:
- lang: eng
text: Huge body of evidences demonstrated that volatile anesthetics affect the hippocampal
neurogenesis and neurocognitive functions, and most of them showed impairment
at anesthetic dose. Here, we investigated the effect of low dose (1.8%) sevoflurane
on hippocampal neurogenesis and dentate gyrus-dependent learning. Neonatal rats
at postnatal day 4 to 6 (P4-6) were treated with 1.8% sevoflurane for 6 hours.
Neurogenesis was quantified by bromodeoxyuridine labeling and electrophysiology
recording. Four and seven weeks after treatment, the Morris water maze and contextual-fear
discrimination learning tests were performed to determine the influence on spatial
learning and pattern separation. A 6-hour treatment with 1.8% sevoflurane promoted
hippocampal neurogenesis and increased the survival of newborn cells and the proportion
of immature granular cells in the dentate gyrus of neonatal rats. Sevoflurane-treated
rats performed better during the training days of the Morris water maze test and
in contextual-fear discrimination learning test. These results suggest that a
subanesthetic dose of sevoflurane promotes hippocampal neurogenesis in neonatal
rats and facilitates their performance in dentate gyrus-dependent learning tasks.
article_processing_charge: No
article_type: original
author:
- first_name: Chong
full_name: Chen, Chong
id: 3DFD581A-F248-11E8-B48F-1D18A9856A87
last_name: Chen
- first_name: Chao
full_name: Wang, Chao
last_name: Wang
- first_name: Xuan
full_name: Zhao, Xuan
last_name: Zhao
- first_name: Tao
full_name: Zhou, Tao
last_name: Zhou
- first_name: Dao
full_name: Xu, Dao
last_name: Xu
- first_name: Zhi
full_name: Wang, Zhi
last_name: Wang
- first_name: Ying
full_name: Wang, Ying
last_name: Wang
citation:
ama: Chen C, Wang C, Zhao X, et al. Low-dose sevoflurane promoteshippocampal neurogenesis
and facilitates the development of dentate gyrus-dependent learning in neonatal
rats. ASN Neuro. 2015;7(2). doi:10.1177/1759091415575845
apa: Chen, C., Wang, C., Zhao, X., Zhou, T., Xu, D., Wang, Z., & Wang, Y. (2015).
Low-dose sevoflurane promoteshippocampal neurogenesis and facilitates the development
of dentate gyrus-dependent learning in neonatal rats. ASN Neuro. SAGE Publications.
https://doi.org/10.1177/1759091415575845
chicago: Chen, Chong, Chao Wang, Xuan Zhao, Tao Zhou, Dao Xu, Zhi Wang, and Ying
Wang. “Low-Dose Sevoflurane Promoteshippocampal Neurogenesis and Facilitates the
Development of Dentate Gyrus-Dependent Learning in Neonatal Rats.” ASN Neuro.
SAGE Publications, 2015. https://doi.org/10.1177/1759091415575845.
ieee: C. Chen et al., “Low-dose sevoflurane promoteshippocampal neurogenesis
and facilitates the development of dentate gyrus-dependent learning in neonatal
rats,” ASN Neuro, vol. 7, no. 2. SAGE Publications, 2015.
ista: Chen C, Wang C, Zhao X, Zhou T, Xu D, Wang Z, Wang Y. 2015. Low-dose sevoflurane
promoteshippocampal neurogenesis and facilitates the development of dentate gyrus-dependent
learning in neonatal rats. ASN Neuro. 7(2).
mla: Chen, Chong, et al. “Low-Dose Sevoflurane Promoteshippocampal Neurogenesis
and Facilitates the Development of Dentate Gyrus-Dependent Learning in Neonatal
Rats.” ASN Neuro, vol. 7, no. 2, SAGE Publications, 2015, doi:10.1177/1759091415575845.
short: C. Chen, C. Wang, X. Zhao, T. Zhou, D. Xu, Z. Wang, Y. Wang, ASN Neuro 7
(2015).
date_created: 2018-12-11T11:54:16Z
date_published: 2015-04-13T00:00:00Z
date_updated: 2025-09-23T09:31:50Z
day: '13'
ddc:
- '570'
department:
- _id: PeJo
doi: 10.1177/1759091415575845
external_id:
isi:
- '000353223200002'
file:
- access_level: open_access
checksum: 53e16bd3fc2ae2c0d7de9164626c37aa
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:14:08Z
date_updated: 2020-07-14T12:45:18Z
file_id: '5057'
file_name: IST-2016-456-v1+1_ASN_Neuro-2015-Chen-.pdf
file_size: 1146814
relation: main_file
file_date_updated: 2020-07-14T12:45:18Z
has_accepted_license: '1'
intvolume: ' 7'
isi: 1
issue: '2'
language:
- iso: eng
license: https://creativecommons.org/licenses/by/3.0/
month: '04'
oa: 1
oa_version: Published Version
publication: ASN Neuro
publication_status: published
publisher: SAGE Publications
publist_id: '5269'
pubrep_id: '456'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Low-dose sevoflurane promoteshippocampal neurogenesis and facilitates the development
of dentate gyrus-dependent learning in neonatal rats
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/3.0/legalcode
name: Creative Commons Attribution 3.0 Unported (CC BY 3.0)
short: CC BY (3.0)
type: journal_article
user_id: 317138e5-6ab7-11ef-aa6d-ffef3953e345
volume: 7
year: '2015'
...