---
_id: '1118'
abstract:
- lang: eng
text: Sharp wave-ripple (SWR) oscillations play a key role in memory consolidation
during non-rapid eye movement sleep, immobility, and consummatory behavior. However,
whether temporally modulated synaptic excitation or inhibition underlies the ripples
is controversial. To address this question, we performed simultaneous recordings
of excitatory and inhibitory postsynaptic currents (EPSCs and IPSCs) and local
field potentials (LFPs) in the CA1 region of awake mice in vivo. During SWRs,
inhibition dominated over excitation, with a peak conductance ratio of 4.1 ± 0.5.
Furthermore, the amplitude of SWR-associated IPSCs was positively correlated with
SWR magnitude, whereas that of EPSCs was not. Finally, phase analysis indicated
that IPSCs were phase-locked to individual ripple cycles, whereas EPSCs were uniformly
distributed in phase space. Optogenetic inhibition indicated that PV+ interneurons
provided a major contribution to SWR-associated IPSCs. Thus, phasic inhibition,
but not excitation, shapes SWR oscillations in the hippocampal CA1 region in vivo.
acknowledged_ssus:
- _id: M-Shop
- _id: ScienComp
- _id: PreCl
article_processing_charge: No
author:
- first_name: Jian
full_name: Gan, Jian
id: 3614E438-F248-11E8-B48F-1D18A9856A87
last_name: Gan
- first_name: Shih-Ming
full_name: Weng, Shih-Ming
id: 2F9C5AC8-F248-11E8-B48F-1D18A9856A87
last_name: Weng
- first_name: Alejandro
full_name: Pernia-Andrade, Alejandro
id: 36963E98-F248-11E8-B48F-1D18A9856A87
last_name: Pernia-Andrade
- first_name: Jozsef L
full_name: Csicsvari, Jozsef L
id: 3FA14672-F248-11E8-B48F-1D18A9856A87
last_name: Csicsvari
orcid: 0000-0002-5193-4036
- 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: Gan J, Weng S-M, Pernia-Andrade A, Csicsvari JL, Jonas PM. Phase-locked inhibition,
but not excitation, underlies hippocampal ripple oscillations in awake mice in
vivo. Neuron. 2017;93(2):308-314. doi:10.1016/j.neuron.2016.12.018
apa: Gan, J., Weng, S.-M., Pernia-Andrade, A., Csicsvari, J. L., & Jonas, P.
M. (2017). Phase-locked inhibition, but not excitation, underlies hippocampal
ripple oscillations in awake mice in vivo. Neuron. Elsevier. https://doi.org/10.1016/j.neuron.2016.12.018
chicago: Gan, Jian, Shih-Ming Weng, Alejandro Pernia-Andrade, Jozsef L Csicsvari,
and Peter M Jonas. “Phase-Locked Inhibition, but Not Excitation, Underlies Hippocampal
Ripple Oscillations in Awake Mice in Vivo.” Neuron. Elsevier, 2017. https://doi.org/10.1016/j.neuron.2016.12.018.
ieee: J. Gan, S.-M. Weng, A. Pernia-Andrade, J. L. Csicsvari, and P. M. Jonas, “Phase-locked
inhibition, but not excitation, underlies hippocampal ripple oscillations in awake
mice in vivo,” Neuron, vol. 93, no. 2. Elsevier, pp. 308–314, 2017.
ista: Gan J, Weng S-M, Pernia-Andrade A, Csicsvari JL, Jonas PM. 2017. Phase-locked
inhibition, but not excitation, underlies hippocampal ripple oscillations in awake
mice in vivo. Neuron. 93(2), 308–314.
mla: Gan, Jian, et al. “Phase-Locked Inhibition, but Not Excitation, Underlies Hippocampal
Ripple Oscillations in Awake Mice in Vivo.” Neuron, vol. 93, no. 2, Elsevier,
2017, pp. 308–14, doi:10.1016/j.neuron.2016.12.018.
short: J. Gan, S.-M. Weng, A. Pernia-Andrade, J.L. Csicsvari, P.M. Jonas, Neuron
93 (2017) 308–314.
date_created: 2018-12-11T11:50:15Z
date_published: 2017-01-18T00:00:00Z
date_updated: 2025-04-15T07:20:01Z
day: '18'
ddc:
- '571'
department:
- _id: PeJo
- _id: JoCs
doi: 10.1016/j.neuron.2016.12.018
ec_funded: 1
external_id:
isi:
- '000396428200010'
file:
- access_level: open_access
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:08:56Z
date_updated: 2018-12-12T10:08:56Z
file_id: '4719'
file_name: IST-2017-752-v1+1_1-s2.0-S0896627316309606-main.pdf
file_size: 2738950
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file_date_updated: 2018-12-12T10:08:56Z
has_accepted_license: '1'
intvolume: ' 93'
isi: 1
issue: '2'
language:
- iso: eng
month: '01'
oa: 1
oa_version: Published Version
page: 308 - 314
project:
- _id: 25C26B1E-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: P24909-B24
name: Mechanisms of transmitter release at GABAergic synapses
- _id: 25C0F108-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '268548'
name: Nanophysiology of fast-spiking, parvalbumin-expressing GABAergic interneurons
publication: Neuron
publication_status: published
publisher: Elsevier
publist_id: '6244'
pubrep_id: '752'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Phase-locked inhibition, but not excitation, underlies hippocampal ripple oscillations
in awake mice in vivo
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: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 93
year: '2017'
...
---
_id: '1616'
abstract:
- lang: eng
text: The hippocampus plays a key role in learning and memory. Previous studies
suggested that the main types of principal neurons, dentate gyrus granule cells
(GCs), CA3 pyramidal neurons, and CA1 pyramidal neurons, differ in their activity
pattern, with sparse firing in GCs and more frequent firing in CA3 and CA1 pyramidal
neurons. It has been assumed but never shown that such different activity may
be caused by differential synaptic excitation. To test this hypothesis, we performed
high-resolution whole-cell patch-clamp recordings in anesthetized rats in vivo.
In contrast to previous in vitro data, both CA3 and CA1 pyramidal neurons fired
action potentials spontaneously, with a frequency of ∼3–6 Hz, whereas GCs were
silent. Furthermore, both CA3 and CA1 cells primarily fired in bursts. To determine
the underlying mechanisms, we quantitatively assessed the frequency of spontaneous
excitatory synaptic input, the passive membrane properties, and the active membrane
characteristics. Surprisingly, GCs showed comparable synaptic excitation to CA3
and CA1 cells and the highest ratio of excitation versus hyperpolarizing inhibition.
Thus, differential synaptic excitation is not responsible for differences in firing.
Moreover, the three types of hippocampal neurons markedly differed in their passive
properties. While GCs showed the most negative membrane potential, CA3 pyramidal
neurons had the highest input resistance and the slowest membrane time constant.
The three types of neurons also differed in the active membrane characteristics.
GCs showed the highest action potential threshold, but displayed the largest gain
of the input-output curves. In conclusion, our results reveal that differential
firing of the three main types of hippocampal principal neurons in vivo is not
primarily caused by differences in the characteristics of the synaptic input,
but by the distinct properties of synaptic integration and input-output transformation.
acknowledgement: "The authors thank Jose Guzman for critically reading prior versions
of the manuscript. They also thank T. Asenov for\r\nengineering mechanical devices,
A. Schlögl for efficient pro-gramming, F. Marr for technical assistance, and E. Kramberger
for manuscript editing."
article_processing_charge: No
author:
- first_name: Janina
full_name: Kowalski, Janina
id: 3F3CA136-F248-11E8-B48F-1D18A9856A87
last_name: Kowalski
- first_name: Jian
full_name: Gan, Jian
id: 3614E438-F248-11E8-B48F-1D18A9856A87
last_name: Gan
- first_name: Peter M
full_name: Jonas, Peter M
id: 353C1B58-F248-11E8-B48F-1D18A9856A87
last_name: Jonas
orcid: 0000-0001-5001-4804
- first_name: Alejandro
full_name: Pernia-Andrade, Alejandro
id: 36963E98-F248-11E8-B48F-1D18A9856A87
last_name: Pernia-Andrade
citation:
ama: Kowalski J, Gan J, Jonas PM, Pernia-Andrade A. Intrinsic membrane properties
determine hippocampal differential firing pattern in vivo in anesthetized rats.
Hippocampus. 2016;26(5):668-682. doi:10.1002/hipo.22550
apa: Kowalski, J., Gan, J., Jonas, P. M., & Pernia-Andrade, A. (2016). Intrinsic
membrane properties determine hippocampal differential firing pattern in vivo
in anesthetized rats. Hippocampus. Wiley. https://doi.org/10.1002/hipo.22550
chicago: Kowalski, Janina, Jian Gan, Peter M Jonas, and Alejandro Pernia-Andrade.
“Intrinsic Membrane Properties Determine Hippocampal Differential Firing Pattern
in Vivo in Anesthetized Rats.” Hippocampus. Wiley, 2016. https://doi.org/10.1002/hipo.22550.
ieee: J. Kowalski, J. Gan, P. M. Jonas, and A. Pernia-Andrade, “Intrinsic membrane
properties determine hippocampal differential firing pattern in vivo in anesthetized
rats,” Hippocampus, vol. 26, no. 5. Wiley, pp. 668–682, 2016.
ista: Kowalski J, Gan J, Jonas PM, Pernia-Andrade A. 2016. Intrinsic membrane properties
determine hippocampal differential firing pattern in vivo in anesthetized rats.
Hippocampus. 26(5), 668–682.
mla: Kowalski, Janina, et al. “Intrinsic Membrane Properties Determine Hippocampal
Differential Firing Pattern in Vivo in Anesthetized Rats.” Hippocampus,
vol. 26, no. 5, Wiley, 2016, pp. 668–82, doi:10.1002/hipo.22550.
short: J. Kowalski, J. Gan, P.M. Jonas, A. Pernia-Andrade, Hippocampus 26 (2016)
668–682.
corr_author: '1'
date_created: 2018-12-11T11:53:03Z
date_published: 2016-05-01T00:00:00Z
date_updated: 2025-09-18T10:58:31Z
day: '01'
ddc:
- '570'
department:
- _id: PeJo
doi: 10.1002/hipo.22550
external_id:
isi:
- '000374666700011'
file:
- access_level: open_access
checksum: 284b72b12fbe15474833ed3d4549f86b
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:13:47Z
date_updated: 2020-07-14T12:45:07Z
file_id: '5033'
file_name: IST-2016-469-v1+1_Kowalski_et_al-Hippocampus.pdf
file_size: 905348
relation: main_file
file_date_updated: 2020-07-14T12:45:07Z
has_accepted_license: '1'
intvolume: ' 26'
isi: 1
issue: '5'
language:
- iso: eng
month: '05'
oa: 1
oa_version: Published Version
page: 668 - 682
publication: Hippocampus
publication_identifier:
eissn:
- 1098-1063
issn:
- 1050-9631
publication_status: published
publisher: Wiley
publist_id: '5550'
pubrep_id: '469'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Intrinsic membrane properties determine hippocampal differential firing pattern
in vivo in anesthetized rats
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: 317138e5-6ab7-11ef-aa6d-ffef3953e345
volume: 26
year: '2016'
...
---
_id: '2062'
abstract:
- lang: eng
text: The success story of fast-spiking, parvalbumin-positive (PV+) GABAergic interneurons
(GABA, γ-aminobutyric acid) in the mammalian central nervous system is noteworthy.
In 1995, the properties of these interneurons were completely unknown. Twenty
years later, thanks to the massive use of subcellular patch-clamp techniques,
simultaneous multiple-cell recording, optogenetics, in vivo measurements, and
computational approaches, our knowledge about PV+ interneurons became more extensive
than for several types of pyramidal neurons. These findings have implications
beyond the “small world” of basic research on GABAergic cells. For example, the
results provide a first proof of principle that neuroscientists might be able
to close the gaps between the molecular, cellular, network, and behavioral levels,
representing one of the main challenges at the present time. Furthermore, the
results may form the basis for PV+ interneurons as therapeutic targets for brain
disease in the future. However, much needs to be learned about the basic function
of these interneurons before clinical neuroscientists will be able to use PV+
interneurons for therapeutic purposes.
article_number: '1255263'
article_processing_charge: No
author:
- first_name: Hua
full_name: Hu, Hua
id: 4AC0145C-F248-11E8-B48F-1D18A9856A87
last_name: Hu
- first_name: Jian
full_name: Gan, Jian
id: 3614E438-F248-11E8-B48F-1D18A9856A87
last_name: Gan
- 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: 'Hu H, Gan J, Jonas PM. Fast-spiking parvalbumin^+ GABAergic interneurons:
From cellular design to microcircuit function. Science. 2014;345(6196).
doi:10.1126/science.1255263'
apa: 'Hu, H., Gan, J., & Jonas, P. M. (2014). Fast-spiking parvalbumin^+ GABAergic
interneurons: From cellular design to microcircuit function. Science. American
Association for the Advancement of Science. https://doi.org/10.1126/science.1255263'
chicago: 'Hu, Hua, Jian Gan, and Peter M Jonas. “Fast-Spiking Parvalbumin^+ GABAergic
Interneurons: From Cellular Design to Microcircuit Function.” Science.
American Association for the Advancement of Science, 2014. https://doi.org/10.1126/science.1255263.'
ieee: 'H. Hu, J. Gan, and P. M. Jonas, “Fast-spiking parvalbumin^+ GABAergic interneurons:
From cellular design to microcircuit function,” Science, vol. 345, no.
6196. American Association for the Advancement of Science, 2014.'
ista: 'Hu H, Gan J, Jonas PM. 2014. Fast-spiking parvalbumin^+ GABAergic interneurons:
From cellular design to microcircuit function. Science. 345(6196), 1255263.'
mla: 'Hu, Hua, et al. “Fast-Spiking Parvalbumin^+ GABAergic Interneurons: From Cellular
Design to Microcircuit Function.” Science, vol. 345, no. 6196, 1255263,
American Association for the Advancement of Science, 2014, doi:10.1126/science.1255263.'
short: H. Hu, J. Gan, P.M. Jonas, Science 345 (2014).
corr_author: '1'
date_created: 2018-12-11T11:55:29Z
date_published: 2014-08-01T00:00:00Z
date_updated: 2025-09-29T11:48:03Z
day: '01'
ddc:
- '570'
department:
- _id: PeJo
doi: 10.1126/science.1255263
ec_funded: 1
external_id:
isi:
- '000339651300036'
file:
- access_level: open_access
checksum: a0036a589037d37e86364fa25cc0a82f
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:16:00Z
date_updated: 2020-07-14T12:45:27Z
file_id: '5185'
file_name: IST-2017-821-v1+1_1255263JonasPVReviewTextR_Final.pdf
file_size: 215514
relation: main_file
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checksum: e1f57d2713725449cb898fdcb8ef47b8
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:16:01Z
date_updated: 2020-07-14T12:45:27Z
file_id: '5186'
file_name: IST-2017-821-v1+2_1255263JonasPVReviewFigures_Final.pdf
file_size: 1732723
relation: main_file
file_date_updated: 2020-07-14T12:45:27Z
has_accepted_license: '1'
intvolume: ' 345'
isi: 1
issue: '6196'
language:
- iso: eng
month: '08'
oa: 1
oa_version: Submitted Version
project:
- _id: 25C26B1E-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: P24909-B24
name: Mechanisms of transmitter release at GABAergic synapses
- _id: 25C0F108-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '268548'
name: Nanophysiology of fast-spiking, parvalbumin-expressing GABAergic interneurons
publication: Science
publication_status: published
publisher: American Association for the Advancement of Science
publist_id: '4984'
pubrep_id: '821'
quality_controlled: '1'
scopus_import: '1'
status: public
title: 'Fast-spiking parvalbumin^+ GABAergic interneurons: From cellular design to
microcircuit function'
type: journal_article
user_id: 317138e5-6ab7-11ef-aa6d-ffef3953e345
volume: 345
year: '2014'
...