---
_id: '10816'
abstract:
- lang: eng
text: Pattern separation is a fundamental brain computation that converts small
differences in input patterns into large differences in output patterns. Several
synaptic mechanisms of pattern separation have been proposed, including code expansion,
inhibition and plasticity; however, which of these mechanisms play a role in the
entorhinal cortex (EC)–dentate gyrus (DG)–CA3 circuit, a classical pattern separation
circuit, remains unclear. Here we show that a biologically realistic, full-scale
EC–DG–CA3 circuit model, including granule cells (GCs) and parvalbumin-positive
inhibitory interneurons (PV+-INs) in the DG, is an efficient pattern separator.
Both external gamma-modulated inhibition and internal lateral inhibition mediated
by PV+-INs substantially contributed to pattern separation. Both local connectivity
and fast signaling at GC–PV+-IN synapses were important for maximum effectiveness.
Similarly, mossy fiber synapses with conditional detonator properties contributed
to pattern separation. By contrast, perforant path synapses with Hebbian synaptic
plasticity and direct EC–CA3 connection shifted the network towards pattern completion.
Our results demonstrate that the specific properties of cells and synapses optimize
higher-order computations in biological networks and might be useful to improve
the deep learning capabilities of technical networks.
acknowledged_ssus:
- _id: SSU
acknowledgement: We thank A. Aertsen, N. Kopell, W. Maass, A. Roth, F. Stella and
T. Vogels for critically reading earlier versions of the manuscript. We are grateful
to F. Marr and C. Altmutter for excellent technical assistance, E. Kralli-Beller
for manuscript editing, and the Scientific Service Units of IST Austria for efficient
support. Finally, we thank T. Carnevale, L. Erdös, M. Hines, D. Nykamp and D. Schröder
for useful discussions, and R. Friedrich and S. Wiechert for sharing unpublished
data. This project received funding from the European Research Council (ERC) under
the European Union’s Horizon 2020 research and innovation programme (grant agreement
no. 692692, P.J.) and the Fond zur Förderung der Wissenschaftlichen Forschung (Z
312-B27, Wittgenstein award to P.J. and P 31815 to S.J.G.).
article_processing_charge: No
article_type: original
author:
- first_name: José
full_name: Guzmán, José
id: 30CC5506-F248-11E8-B48F-1D18A9856A87
last_name: Guzmán
orcid: 0000-0003-2209-5242
- first_name: Alois
full_name: Schlögl, Alois
id: 45BF87EE-F248-11E8-B48F-1D18A9856A87
last_name: Schlögl
orcid: 0000-0002-5621-8100
- first_name: 'Claudia '
full_name: 'Espinoza Martinez, Claudia '
id: 31FFEE2E-F248-11E8-B48F-1D18A9856A87
last_name: Espinoza Martinez
orcid: 0000-0003-4710-2082
- first_name: Xiaomin
full_name: Zhang, Xiaomin
id: 423EC9C2-F248-11E8-B48F-1D18A9856A87
last_name: Zhang
- first_name: Benjamin
full_name: Suter, Benjamin
id: 4952F31E-F248-11E8-B48F-1D18A9856A87
last_name: Suter
orcid: 0000-0002-9885-6936
- 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: Guzmán J, Schlögl A, Espinoza Martinez C, Zhang X, Suter B, Jonas PM. How connectivity
rules and synaptic properties shape the efficacy of pattern separation in the
entorhinal cortex–dentate gyrus–CA3 network. Nature Computational Science.
2021;1(12):830-842. doi:10.1038/s43588-021-00157-1
apa: Guzmán, J., Schlögl, A., Espinoza Martinez, C., Zhang, X., Suter, B., &
Jonas, P. M. (2021). How connectivity rules and synaptic properties shape the
efficacy of pattern separation in the entorhinal cortex–dentate gyrus–CA3 network.
Nature Computational Science. Springer Nature. https://doi.org/10.1038/s43588-021-00157-1
chicago: Guzmán, José, Alois Schlögl, Claudia Espinoza Martinez, Xiaomin Zhang,
Benjamin Suter, and Peter M Jonas. “How Connectivity Rules and Synaptic Properties
Shape the Efficacy of Pattern Separation in the Entorhinal Cortex–Dentate Gyrus–CA3
Network.” Nature Computational Science. Springer Nature, 2021. https://doi.org/10.1038/s43588-021-00157-1.
ieee: J. Guzmán, A. Schlögl, C. Espinoza Martinez, X. Zhang, B. Suter, and P. M.
Jonas, “How connectivity rules and synaptic properties shape the efficacy of pattern
separation in the entorhinal cortex–dentate gyrus–CA3 network,” Nature Computational
Science, vol. 1, no. 12. Springer Nature, pp. 830–842, 2021.
ista: Guzmán J, Schlögl A, Espinoza Martinez C, Zhang X, Suter B, Jonas PM. 2021.
How connectivity rules and synaptic properties shape the efficacy of pattern separation
in the entorhinal cortex–dentate gyrus–CA3 network. Nature Computational Science.
1(12), 830–842.
mla: Guzmán, José, et al. “How Connectivity Rules and Synaptic Properties Shape
the Efficacy of Pattern Separation in the Entorhinal Cortex–Dentate Gyrus–CA3
Network.” Nature Computational Science, vol. 1, no. 12, Springer Nature,
2021, pp. 830–42, doi:10.1038/s43588-021-00157-1.
short: J. Guzmán, A. Schlögl, C. Espinoza Martinez, X. Zhang, B. Suter, P.M. Jonas,
Nature Computational Science 1 (2021) 830–842.
date_created: 2022-03-04T08:32:36Z
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date_updated: 2023-08-10T22:30:10Z
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call_identifier: FWF
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publication: Nature Computational Science
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relation: software
status: public
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title: How connectivity rules and synaptic properties shape the efficacy of pattern
separation in the entorhinal cortex–dentate gyrus–CA3 network
type: journal_article
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year: '2021'
...
---
_id: '10110'
abstract:
- lang: eng
text: Pattern separation is a fundamental brain computation that converts small
differences in input patterns into large differences in output patterns. Several
synaptic mechanisms of pattern separation have been proposed, including code expansion,
inhibition and plasticity; however, which of these mechanisms play a role in the
entorhinal cortex (EC)–dentate gyrus (DG)–CA3 circuit, a classical pattern separation
circuit, remains unclear. Here we show that a biologically realistic, full-scale
EC–DG–CA3 circuit model, including granule cells (GCs) and parvalbumin-positive
inhibitory interneurons (PV+-INs) in the DG, is an efficient pattern separator.
Both external gamma-modulated inhibition and internal lateral inhibition mediated
by PV+-INs substantially contributed to pattern separation. Both local connectivity
and fast signaling at GC–PV+-IN synapses were important for maximum effectiveness.
Similarly, mossy fiber synapses with conditional detonator properties contributed
to pattern separation. By contrast, perforant path synapses with Hebbian synaptic
plasticity and direct EC–CA3 connection shifted the network towards pattern completion.
Our results demonstrate that the specific properties of cells and synapses optimize
higher-order computations in biological networks and might be useful to improve
the deep learning capabilities of technical networks.
author:
- first_name: José
full_name: Guzmán, José
id: 30CC5506-F248-11E8-B48F-1D18A9856A87
last_name: Guzmán
orcid: 0000-0003-2209-5242
- first_name: Alois
full_name: Schlögl, Alois
id: 45BF87EE-F248-11E8-B48F-1D18A9856A87
last_name: Schlögl
orcid: 0000-0002-5621-8100
- first_name: 'Claudia '
full_name: 'Espinoza Martinez, Claudia '
id: 31FFEE2E-F248-11E8-B48F-1D18A9856A87
last_name: Espinoza Martinez
orcid: 0000-0003-4710-2082
- first_name: Xiaomin
full_name: Zhang, Xiaomin
id: 423EC9C2-F248-11E8-B48F-1D18A9856A87
last_name: Zhang
- first_name: Benjamin
full_name: Suter, Benjamin
id: 4952F31E-F248-11E8-B48F-1D18A9856A87
last_name: Suter
orcid: 0000-0002-9885-6936
- 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: Guzmán J, Schlögl A, Espinoza Martinez C, Zhang X, Suter B, Jonas PM. How connectivity
rules and synaptic properties shape the efficacy of pattern separation in the
entorhinal cortex–dentate gyrus–CA3 network. 2021. doi:10.15479/AT:ISTA:10110
apa: Guzmán, J., Schlögl, A., Espinoza Martinez, C., Zhang, X., Suter, B., &
Jonas, P. M. (2021). How connectivity rules and synaptic properties shape the
efficacy of pattern separation in the entorhinal cortex–dentate gyrus–CA3 network.
IST Austria. https://doi.org/10.15479/AT:ISTA:10110
chicago: Guzmán, José, Alois Schlögl, Claudia Espinoza Martinez, Xiaomin Zhang,
Benjamin Suter, and Peter M Jonas. “How Connectivity Rules and Synaptic Properties
Shape the Efficacy of Pattern Separation in the Entorhinal Cortex–Dentate Gyrus–CA3
Network.” IST Austria, 2021. https://doi.org/10.15479/AT:ISTA:10110.
ieee: J. Guzmán, A. Schlögl, C. Espinoza Martinez, X. Zhang, B. Suter, and P. M.
Jonas, “How connectivity rules and synaptic properties shape the efficacy of pattern
separation in the entorhinal cortex–dentate gyrus–CA3 network.” IST Austria, 2021.
ista: Guzmán J, Schlögl A, Espinoza Martinez C, Zhang X, Suter B, Jonas PM. 2021.
How connectivity rules and synaptic properties shape the efficacy of pattern separation
in the entorhinal cortex–dentate gyrus–CA3 network, IST Austria, 10.15479/AT:ISTA:10110.
mla: Guzmán, José, et al. How Connectivity Rules and Synaptic Properties Shape
the Efficacy of Pattern Separation in the Entorhinal Cortex–Dentate Gyrus–CA3
Network. IST Austria, 2021, doi:10.15479/AT:ISTA:10110.
short: J. Guzmán, A. Schlögl, C. Espinoza Martinez, X. Zhang, B. Suter, P.M. Jonas,
(2021).
date_created: 2021-10-08T06:44:22Z
date_published: 2021-12-16T00:00:00Z
date_updated: 2024-03-25T23:30:07Z
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title: How connectivity rules and synaptic properties shape the efficacy of pattern
separation in the entorhinal cortex–dentate gyrus–CA3 network
tmp:
legal_code_url: https://www.gnu.org/licenses/gpl-3.0.en.html
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year: '2021'
...
---
_id: '6363'
abstract:
- lang: eng
text: "Distinguishing between similar experiences is achieved by the brain
\ in a process called pattern separation. In the hippocampus, pattern
\ separation reduces the interference of memories and increases the storage
capacity by decorrelating similar inputs patterns of neuronal activity into
\ non-overlapping output firing patterns. Winners-take-all (WTA) mechanism
\ is a theoretical model for pattern separation in which a \"winner\"
\ cell suppresses the activity of the neighboring neurons through feedback
inhibition. However, if the network properties of the dentate gyrus support WTA
as a biologically conceivable model remains unknown. Here, we showed that the
connectivity rules of PV+interneurons and their synaptic properties are optimizedfor
efficient pattern separation. We found using multiple whole-cell in vitrorecordings
that PV+interneurons mainly connect to granule cells (GC) through lateral inhibition,
a form of feedback inhibition in which a GC inhibits other GCs but not
\ itself through the activation of PV+interneurons. Thus, lateral inhibition
between GC–PV+interneurons was ~10 times more abundant than recurrent connections.
Furthermore, the GC–PV+interneuron connectivity was more spatially confined
\ but less abundant than PV+interneurons–GC connectivity, leading to an
\ asymmetrical distribution of excitatory and inhibitory connectivity. Our
network model of the dentate gyrus with incorporated real connectivity rules efficiently
decorrelates neuronal activity patterns using WTA as the primary mechanism.
\ This process relied on lateral inhibition, fast-signaling properties of
\ PV+interneurons and the asymmetrical distribution of excitatory and inhibitory
connectivity. Finally, we found that silencing the activity of PV+interneurons
in vivoleads to acute deficits in discrimination between similar environments,
suggesting that PV+interneuron networks are necessary for behavioral relevant
computations. Our results demonstrate that PV+interneurons possess unique
connectivity and fast signaling properties that confer to the dentate
\ gyrus network properties that allow the emergence of pattern separation. Thus,
our results contribute to the knowledge of how specific forms of network organization
underlie sophisticated types of information processing. \r\n"
alternative_title:
- ISTA Thesis
article_processing_charge: No
author:
- first_name: 'Claudia '
full_name: 'Espinoza Martinez, Claudia '
id: 31FFEE2E-F248-11E8-B48F-1D18A9856A87
last_name: Espinoza Martinez
orcid: 0000-0003-4710-2082
citation:
ama: Espinoza Martinez C. Parvalbumin+ interneurons enable efficient pattern separation
in hippocampal microcircuits. 2019. doi:10.15479/AT:ISTA:6363
apa: Espinoza Martinez, C. (2019). Parvalbumin+ interneurons enable efficient
pattern separation in hippocampal microcircuits. Institute of Science and
Technology Austria. https://doi.org/10.15479/AT:ISTA:6363
chicago: Espinoza Martinez, Claudia . “Parvalbumin+ Interneurons Enable Efficient
Pattern Separation in Hippocampal Microcircuits.” Institute of Science and Technology
Austria, 2019. https://doi.org/10.15479/AT:ISTA:6363.
ieee: C. Espinoza Martinez, “Parvalbumin+ interneurons enable efficient pattern
separation in hippocampal microcircuits,” Institute of Science and Technology
Austria, 2019.
ista: Espinoza Martinez C. 2019. Parvalbumin+ interneurons enable efficient pattern
separation in hippocampal microcircuits. Institute of Science and Technology Austria.
mla: Espinoza Martinez, Claudia. Parvalbumin+ Interneurons Enable Efficient Pattern
Separation in Hippocampal Microcircuits. Institute of Science and Technology
Austria, 2019, doi:10.15479/AT:ISTA:6363.
short: C. Espinoza Martinez, Parvalbumin+ Interneurons Enable Efficient Pattern
Separation in Hippocampal Microcircuits, Institute of Science and Technology Austria,
2019.
date_created: 2019-04-30T11:56:10Z
date_published: 2019-04-30T00:00:00Z
date_updated: 2023-09-15T12:03:48Z
day: '30'
ddc:
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degree_awarded: PhD
department:
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doi: 10.15479/AT:ISTA:6363
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page: '140'
publication_identifier:
isbn:
- 978-3-99078-000-8
issn:
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publisher: Institute of Science and Technology Austria
related_material:
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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: Parvalbumin+ interneurons enable efficient pattern separation in hippocampal
microcircuits
type: dissertation
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
year: '2019'
...
---
_id: '21'
abstract:
- lang: eng
text: Parvalbumin-positive (PV+) GABAergic interneurons in hippocampal microcircuits
are thought to play a key role in several higher network functions, such as feedforward
and feedback inhibition, network oscillations, and pattern separation. Fast lateral
inhibition mediated by GABAergic interneurons may implement a winner-takes-all
mechanism in the hippocampal input layer. However, it is not clear whether the
functional connectivity rules of granule cells (GCs) and interneurons in the dentate
gyrus are consistent with such a mechanism. Using simultaneous patch-clamp recordings
from up to seven GCs and up to four PV+ interneurons in the dentate gyrus, we
find that connectivity is structured in space, synapse-specific, and enriched
in specific disynaptic motifs. In contrast to the neocortex, lateral inhibition
in the dentate gyrus (in which a GC inhibits neighboring GCs via a PV+ interneuron)
is ~ 10-times more abundant than recurrent inhibition (in which a GC inhibits
itself). Thus, unique connectivity rules may enable the dentate gyrus to perform
specific higher-order computations
acknowledgement: This project received funding from the European Research Council
(ERC) under the European Union’s Horizon 2020 research and innovation programme
(grant agreement No 692692) and the Fond zur Förderung der Wissenschaftlichen Forschung
(Z 312-B27, Wittgenstein award), both to P.J..
article_number: '4605'
article_processing_charge: No
article_type: original
author:
- first_name: 'Claudia '
full_name: 'Espinoza Martinez, Claudia '
id: 31FFEE2E-F248-11E8-B48F-1D18A9856A87
last_name: Espinoza Martinez
orcid: 0000-0003-4710-2082
- first_name: José
full_name: Guzmán, José
id: 30CC5506-F248-11E8-B48F-1D18A9856A87
last_name: Guzmán
orcid: 0000-0003-2209-5242
- 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: Espinoza Martinez C, Guzmán J, Zhang X, Jonas PM. Parvalbumin+ interneurons
obey unique connectivity rules and establish a powerful lateral-inhibition microcircuit
in dentate gyrus. Nature Communications. 2018;9(1). doi:10.1038/s41467-018-06899-3
apa: Espinoza Martinez, C., Guzmán, J., Zhang, X., & Jonas, P. M. (2018). Parvalbumin+
interneurons obey unique connectivity rules and establish a powerful lateral-inhibition
microcircuit in dentate gyrus. Nature Communications. Nature Publishing
Group. https://doi.org/10.1038/s41467-018-06899-3
chicago: Espinoza Martinez, Claudia , José Guzmán, Xiaomin Zhang, and Peter M Jonas.
“Parvalbumin+ Interneurons Obey Unique Connectivity Rules and Establish a Powerful
Lateral-Inhibition Microcircuit in Dentate Gyrus.” Nature Communications.
Nature Publishing Group, 2018. https://doi.org/10.1038/s41467-018-06899-3.
ieee: C. Espinoza Martinez, J. Guzmán, X. Zhang, and P. M. Jonas, “Parvalbumin+
interneurons obey unique connectivity rules and establish a powerful lateral-inhibition
microcircuit in dentate gyrus,” Nature Communications, vol. 9, no. 1. Nature
Publishing Group, 2018.
ista: Espinoza Martinez C, Guzmán J, Zhang X, Jonas PM. 2018. Parvalbumin+ interneurons
obey unique connectivity rules and establish a powerful lateral-inhibition microcircuit
in dentate gyrus. Nature Communications. 9(1), 4605.
mla: Espinoza Martinez, Claudia, et al. “Parvalbumin+ Interneurons Obey Unique Connectivity
Rules and Establish a Powerful Lateral-Inhibition Microcircuit in Dentate Gyrus.”
Nature Communications, vol. 9, no. 1, 4605, Nature Publishing Group, 2018,
doi:10.1038/s41467-018-06899-3.
short: C. Espinoza Martinez, J. Guzmán, X. Zhang, P.M. Jonas, Nature Communications
9 (2018).
date_created: 2018-12-11T11:44:12Z
date_published: 2018-11-02T00:00:00Z
date_updated: 2024-03-25T23:30:16Z
day: '02'
ddc:
- '570'
department:
- _id: PeJo
doi: 10.1038/s41467-018-06899-3
ec_funded: 1
external_id:
isi:
- '000449069700009'
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checksum: 9fe2a63bd95a5067d896c087d07998f3
content_type: application/pdf
creator: dernst
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file_size: 4651930
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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
publication: Nature Communications
publication_status: published
publisher: Nature Publishing Group
publist_id: '8034'
quality_controlled: '1'
related_material:
link:
- description: News on IST Homepage
relation: press_release
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scopus_import: '1'
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title: Parvalbumin+ interneurons obey unique connectivity rules and establish a powerful
lateral-inhibition microcircuit in dentate gyrus
tmp:
image: /images/cc_by.png
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name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
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year: '2018'
...
---
_id: '1845'
abstract:
- lang: eng
text: Based on extrapolation from excitatory synapses, it is often assumed that
depletion of the releasable pool of synaptic vesicles is the main factor underlying
depression at inhibitory synapses. In this issue of Neuron, using subcellular
patch-clamp recording from inhibitory presynaptic terminals, Kawaguchi and Sakaba
(2015) show that at Purkinje cell-deep cerebellar nuclei neuron synapses, changes
in presynaptic action potential waveform substantially contribute to synaptic
depression. Based on extrapolation from excitatory synapses, it is often assumed
that depletion of the releasable pool of synaptic vesicles is the main factor
underlying depression at inhibitory synapses. In this issue of Neuron, using subcellular
patch-clamp recording from inhibitory presynaptic terminals, Kawaguchi and Sakaba
(2015) show that at Purkinje cell-deep cerebellar nuclei neuron synapses, changes
in presynaptic action potential waveform substantially contribute to synaptic
depression.
article_processing_charge: No
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: 'Claudia '
full_name: 'Espinoza Martinez, Claudia '
id: 31FFEE2E-F248-11E8-B48F-1D18A9856A87
last_name: Espinoza Martinez
orcid: 0000-0003-4710-2082
- 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, Espinoza Martinez C, Jonas PM. Excitement about inhibitory presynaptic
terminals. Neuron. 2015;85(6):1149-1151. doi:10.1016/j.neuron.2015.03.006
apa: Vandael, D. H., Espinoza Martinez, C., & Jonas, P. M. (2015). Excitement
about inhibitory presynaptic terminals. Neuron. Elsevier. https://doi.org/10.1016/j.neuron.2015.03.006
chicago: Vandael, David H, Claudia Espinoza Martinez, and Peter M Jonas. “Excitement
about Inhibitory Presynaptic Terminals.” Neuron. Elsevier, 2015. https://doi.org/10.1016/j.neuron.2015.03.006.
ieee: D. H. Vandael, C. Espinoza Martinez, and P. M. Jonas, “Excitement about inhibitory
presynaptic terminals,” Neuron, vol. 85, no. 6. Elsevier, pp. 1149–1151,
2015.
ista: Vandael DH, Espinoza Martinez C, Jonas PM. 2015. Excitement about inhibitory
presynaptic terminals. Neuron. 85(6), 1149–1151.
mla: Vandael, David H., et al. “Excitement about Inhibitory Presynaptic Terminals.”
Neuron, vol. 85, no. 6, Elsevier, 2015, pp. 1149–51, doi:10.1016/j.neuron.2015.03.006.
short: D.H. Vandael, C. Espinoza Martinez, P.M. Jonas, Neuron 85 (2015) 1149–1151.
date_created: 2018-12-11T11:54:19Z
date_published: 2015-03-18T00:00:00Z
date_updated: 2021-10-08T09:07:34Z
day: '18'
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department:
- _id: PeJo
doi: 10.1016/j.neuron.2015.03.006
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title: Excitement about inhibitory presynaptic terminals
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