---
_id: '6849'
abstract:
- lang: eng
text: 'Brain function is mediated by complex dynamical interactions between excitatory
and inhibitory cell types. The Cholecystokinin-expressing inhibitory cells (CCK-interneurons)
are one of the least studied types, despite being suspected to play important
roles in cognitive processes. We studied the network effects of optogenetic silencing
of CCK-interneurons in the CA1 hippocampal area during exploration and sleep states.
The cell firing pattern in response to light pulses allowed us to classify the
recorded neurons in 5 classes, including disinhibited and non-responsive pyramidal
cell and interneurons, and the inhibited interneurons corresponding to the CCK
group. The light application, which inhibited the activity of CCK interneurons
triggered wider changes in the firing dynamics of cells. We observed rate changes
(i.e. remapping) of pyramidal cells during the exploration session in which the
light was applied relative to the previous control session that was not restricted
neither in time nor space to the light delivery. Also, the disinhibited pyramidal
cells had higher increase in bursting than in single spike firing rate as a result
of CCK silencing. In addition, the firing activity patterns during exploratory
periods were more weakly reactivated in sleep for those periods in which CCK-interneuron
were silenced than in the unaffected periods. Furthermore, light pulses during
sleep disrupted the reactivation of recent waking patterns. Hence, silencing CCK
neurons during exploration suppressed the reactivation of waking firing patterns
in sleep and CCK interneuron activity was also required during sleep for the normal
reactivation of waking patterns. These findings demonstrate the involvement of
CCK cells in reactivation-related memory consolidation. An important part of our
analysis was to test the relationship of the identified CCKinterneurons to brain
oscillations. Our findings showed that these cells exhibited different oscillatory
behaviour during anaesthesia and natural waking and sleep conditions. We showed
that: 1) Contrary to the past studies performed under anaesthesia, the identified
CCKinterneurons fired on the descending portion of the theta phase in waking exploration.
2) CCKinterneuron preferred phases around the trough of gamma oscillations. 3)
Contrary to anaesthesia conditions, the average firing rate of the CCK-interneurons
increased around the peak activity of the sharp-wave ripple (SWR) events in natural
sleep, which is congruent with new reports about their functional connectivity.
We also found that light driven CCK-interneuron silencing altered the dynamics
on the CA1 network oscillatory activity: 1) Pyramidal cells negatively shifted
their preferred theta phases when the light was applied, while interneurons responses
were less consistent. 2) As a population, pyramidal cells negatively shifted their
preferred activity during gamma oscillations, albeit we did not find gamma modulation
differences related to the light application when pyramidal cells were subdivided
into the disinhibited and unaffected groups. 3) During the peak of SWR events,
all but the CCK-interneurons had a reduction in their relative firing rate change
during the light application as compared to the change observed at SWR initiation.
Finally, regarding to the place field activity of the recorded pyramidal neurons,
we showed that the disinhibited pyramidal cells had reduced place field similarity,
coherence and spatial information, but only during the light application. The
mechanisms behind such observed behaviours might involve eCB signalling and plastic
changes in CCK-interneuron synapses. In conclusion, the observed changes related
to the light-mediated silencing of CCKinterneurons have unravelled characteristics
of this interneuron subpopulation that might change the understanding not only
of their particular network interactions, but also of the current theories about
the emergence of certain cognitive processes such as place coding needed for navigation
or hippocampus-dependent memory consolidation. '
acknowledged_ssus:
- _id: Bio
- _id: PreCl
- _id: M-Shop
alternative_title:
- ISTA Thesis
article_processing_charge: No
author:
- first_name: Dámaris K
full_name: Rangel Guerrero, Dámaris K
id: 4871BCE6-F248-11E8-B48F-1D18A9856A87
last_name: Rangel Guerrero
orcid: 0000-0002-8602-4374
citation:
ama: Rangel Guerrero DK. The role of CCK-interneurons in regulating hippocampal
network dynamics. 2019. doi:10.15479/AT:ISTA:6849
apa: Rangel Guerrero, D. K. (2019). The role of CCK-interneurons in regulating
hippocampal network dynamics. Institute of Science and Technology Austria.
https://doi.org/10.15479/AT:ISTA:6849
chicago: Rangel Guerrero, Dámaris K. “The Role of CCK-Interneurons in Regulating
Hippocampal Network Dynamics.” Institute of Science and Technology Austria, 2019.
https://doi.org/10.15479/AT:ISTA:6849.
ieee: D. K. Rangel Guerrero, “The role of CCK-interneurons in regulating hippocampal
network dynamics,” Institute of Science and Technology Austria, 2019.
ista: Rangel Guerrero DK. 2019. The role of CCK-interneurons in regulating hippocampal
network dynamics. Institute of Science and Technology Austria.
mla: Rangel Guerrero, Dámaris K. The Role of CCK-Interneurons in Regulating Hippocampal
Network Dynamics. Institute of Science and Technology Austria, 2019, doi:10.15479/AT:ISTA:6849.
short: D.K. Rangel Guerrero, The Role of CCK-Interneurons in Regulating Hippocampal
Network Dynamics, Institute of Science and Technology Austria, 2019.
date_created: 2019-09-06T06:54:16Z
date_published: 2019-09-09T00:00:00Z
date_updated: 2023-09-19T10:01:12Z
day: '09'
ddc:
- '570'
degree_awarded: PhD
department:
- _id: JoCs
doi: 10.15479/AT:ISTA:6849
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page: '97'
publication_identifier:
isbn:
- '9783990780039'
issn:
- 2663-337X
publication_status: published
publisher: Institute of Science and Technology Austria
related_material:
record:
- id: '5914'
relation: part_of_dissertation
status: public
status: public
supervisor:
- first_name: Jozsef L
full_name: Csicsvari, Jozsef L
id: 3FA14672-F248-11E8-B48F-1D18A9856A87
last_name: Csicsvari
orcid: 0000-0002-5193-4036
title: The role of CCK-interneurons in regulating hippocampal network dynamics
type: dissertation
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
year: '2019'
...
---
_id: '5914'
abstract:
- lang: eng
text: With the advent of optogenetics, it became possible to change the activity
of a targeted population of neurons in a temporally controlled manner. To combine
the advantages of 60-channel in vivo tetrode recording and laser-based optogenetics,
we have developed a closed-loop recording system that allows for the actual electrophysiological
signal to be used as a trigger for the laser light mediating the optogenetic intervention.
We have optimized the weight, size, and shape of the corresponding implant to
make it compatible with the size, force, and movements of a behaving mouse, and
we have shown that the system can efficiently block sharp wave ripple (SWR) events
using those events themselves as a trigger. To demonstrate the full potential
of the optogenetic recording system we present a pilot study addressing the contribution
of SWR events to learning in a complex behavioral task.
article_number: e0087
article_processing_charge: No
author:
- first_name: Dámaris K
full_name: Rangel Guerrero, Dámaris K
id: 4871BCE6-F248-11E8-B48F-1D18A9856A87
last_name: Rangel Guerrero
orcid: 0000-0002-8602-4374
- first_name: James G.
full_name: Donnett, James G.
last_name: Donnett
- 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: Krisztián
full_name: Kovács, Krisztián
id: 2AB5821E-F248-11E8-B48F-1D18A9856A87
last_name: Kovács
orcid: 0000-0001-6251-1007
citation:
ama: 'Rangel Guerrero DK, Donnett JG, Csicsvari JL, Kovács K. Tetrode recording
from the hippocampus of behaving mice coupled with four-point-irradiation closed-loop
optogenetics: A technique to study the contribution of Hippocampal SWR events
to learning. eNeuro. 2018;5(4). doi:10.1523/ENEURO.0087-18.2018'
apa: 'Rangel Guerrero, D. K., Donnett, J. G., Csicsvari, J. L., & Kovács, K.
(2018). Tetrode recording from the hippocampus of behaving mice coupled with four-point-irradiation
closed-loop optogenetics: A technique to study the contribution of Hippocampal
SWR events to learning. ENeuro. Society of Neuroscience. https://doi.org/10.1523/ENEURO.0087-18.2018'
chicago: 'Rangel Guerrero, Dámaris K, James G. Donnett, Jozsef L Csicsvari, and
Krisztián Kovács. “Tetrode Recording from the Hippocampus of Behaving Mice Coupled
with Four-Point-Irradiation Closed-Loop Optogenetics: A Technique to Study the
Contribution of Hippocampal SWR Events to Learning.” ENeuro. Society of
Neuroscience, 2018. https://doi.org/10.1523/ENEURO.0087-18.2018.'
ieee: 'D. K. Rangel Guerrero, J. G. Donnett, J. L. Csicsvari, and K. Kovács, “Tetrode
recording from the hippocampus of behaving mice coupled with four-point-irradiation
closed-loop optogenetics: A technique to study the contribution of Hippocampal
SWR events to learning,” eNeuro, vol. 5, no. 4. Society of Neuroscience,
2018.'
ista: 'Rangel Guerrero DK, Donnett JG, Csicsvari JL, Kovács K. 2018. Tetrode recording
from the hippocampus of behaving mice coupled with four-point-irradiation closed-loop
optogenetics: A technique to study the contribution of Hippocampal SWR events
to learning. eNeuro. 5(4), e0087.'
mla: 'Rangel Guerrero, Dámaris K., et al. “Tetrode Recording from the Hippocampus
of Behaving Mice Coupled with Four-Point-Irradiation Closed-Loop Optogenetics:
A Technique to Study the Contribution of Hippocampal SWR Events to Learning.”
ENeuro, vol. 5, no. 4, e0087, Society of Neuroscience, 2018, doi:10.1523/ENEURO.0087-18.2018.'
short: D.K. Rangel Guerrero, J.G. Donnett, J.L. Csicsvari, K. Kovács, ENeuro 5 (2018).
date_created: 2019-02-03T22:59:16Z
date_published: 2018-07-27T00:00:00Z
date_updated: 2024-03-25T23:30:06Z
day: '27'
ddc:
- '570'
department:
- _id: JoCs
doi: 10.1523/ENEURO.0087-18.2018
ec_funded: 1
external_id:
isi:
- '000443994700007'
file:
- access_level: open_access
checksum: f4915d45fc7ad4648b7b7a13fdecca01
content_type: application/pdf
creator: dernst
date_created: 2019-02-05T12:48:36Z
date_updated: 2020-07-14T12:47:13Z
file_id: '5921'
file_name: 2018_ENeuro_Guerrero.pdf
file_size: 3746884
relation: main_file
file_date_updated: 2020-07-14T12:47:13Z
has_accepted_license: '1'
intvolume: ' 5'
isi: 1
issue: '4'
language:
- iso: eng
license: https://creativecommons.org/licenses/by/4.0/
month: '07'
oa: 1
oa_version: Published Version
project:
- _id: 25681D80-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '291734'
name: International IST Postdoc Fellowship Programme
- _id: 257D4372-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: I2072-B27
name: Interneuron plasticity during spatial learning
publication: eNeuro
publication_status: published
publisher: Society of Neuroscience
quality_controlled: '1'
related_material:
record:
- id: '6849'
relation: dissertation_contains
status: public
scopus_import: '1'
status: public
title: 'Tetrode recording from the hippocampus of behaving mice coupled with four-point-irradiation
closed-loop optogenetics: A technique to study the contribution of Hippocampal SWR
events to learning'
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: 5
year: '2018'
...
---
_id: '1279'
abstract:
- lang: eng
text: During hippocampal sharp wave/ripple (SWR) events, previously occurring, sensory
inputdriven neuronal firing patterns are replayed. Such replay is thought to be
important for plasticity- related processes and consolidation of memory traces.
It has previously been shown that the electrical stimulation-induced disruption
of SWR events interferes with learning in rodents in different experimental paradigms.
On the other hand, the cognitive map theory posits that the plastic changes of
the firing of hippocampal place cells constitute the electrophysiological counterpart
of the spatial learning, observable at the behavioral level. Therefore, we tested
whether intact SWR events occurring during the sleep/rest session after the first
exploration of a novel environment are needed for the stabilization of the CA1
code, which process requires plasticity. We found that the newly-formed representation
in the CA1 has the same level of stability with optogenetic SWR blockade as with
a control manipulation that delivered the same amount of light into the brain.
Therefore our results suggest that at least in the case of passive exploratory
behavior, SWR-related plasticity is dispensable for the stability of CA1 ensembles.
acknowledgement: 'The research leading to these results has received funding from
the People Programme (Marie Curie Actions) of the European Union''s Seventh Framework
Programme (FP7/2007-2013) under REA grant agreement n° [291734] via the IST FELLOWSHIP
awarded to Dr. Krisztián A. Kovács and the European Research Council starting grant
(acronym: HIPECMEM Project reference: 281511) awarded to Dr. Jozsef Csicsvari. We
thank Lauri Viljanto for technical help in building the ripple detector.'
article_number: e0164675
author:
- first_name: Krisztián
full_name: Kovács, Krisztián
id: 2AB5821E-F248-11E8-B48F-1D18A9856A87
last_name: Kovács
- first_name: Joseph
full_name: O'Neill, Joseph
id: 426376DC-F248-11E8-B48F-1D18A9856A87
last_name: O'Neill
- first_name: Philipp
full_name: Schönenberger, Philipp
id: 3B9D816C-F248-11E8-B48F-1D18A9856A87
last_name: Schönenberger
- first_name: Markku
full_name: Penttonen, Markku
last_name: Penttonen
- first_name: Dámaris K
full_name: Rangel Guerrero, Dámaris K
id: 4871BCE6-F248-11E8-B48F-1D18A9856A87
last_name: Rangel Guerrero
orcid: 0000-0002-8602-4374
- 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: Kovács K, O’Neill J, Schönenberger P, Penttonen M, Rangel Guerrero DK, Csicsvari
JL. Optogenetically blocking sharp wave ripple events in sleep does not interfere
with the formation of stable spatial representation in the CA1 area of the hippocampus.
PLoS One. 2016;11(10). doi:10.1371/journal.pone.0164675
apa: Kovács, K., O’Neill, J., Schönenberger, P., Penttonen, M., Rangel Guerrero,
D. K., & Csicsvari, J. L. (2016). Optogenetically blocking sharp wave ripple
events in sleep does not interfere with the formation of stable spatial representation
in the CA1 area of the hippocampus. PLoS One. Public Library of Science.
https://doi.org/10.1371/journal.pone.0164675
chicago: Kovács, Krisztián, Joseph O’Neill, Philipp Schönenberger, Markku Penttonen,
Dámaris K Rangel Guerrero, and Jozsef L Csicsvari. “Optogenetically Blocking Sharp
Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial
Representation in the CA1 Area of the Hippocampus.” PLoS One. Public Library
of Science, 2016. https://doi.org/10.1371/journal.pone.0164675.
ieee: K. Kovács, J. O’Neill, P. Schönenberger, M. Penttonen, D. K. Rangel Guerrero,
and J. L. Csicsvari, “Optogenetically blocking sharp wave ripple events in sleep
does not interfere with the formation of stable spatial representation in the
CA1 area of the hippocampus,” PLoS One, vol. 11, no. 10. Public Library
of Science, 2016.
ista: Kovács K, O’Neill J, Schönenberger P, Penttonen M, Rangel Guerrero DK, Csicsvari
JL. 2016. Optogenetically blocking sharp wave ripple events in sleep does not
interfere with the formation of stable spatial representation in the CA1 area
of the hippocampus. PLoS One. 11(10), e0164675.
mla: Kovács, Krisztián, et al. “Optogenetically Blocking Sharp Wave Ripple Events
in Sleep Does Not Interfere with the Formation of Stable Spatial Representation
in the CA1 Area of the Hippocampus.” PLoS One, vol. 11, no. 10, e0164675,
Public Library of Science, 2016, doi:10.1371/journal.pone.0164675.
short: K. Kovács, J. O’Neill, P. Schönenberger, M. Penttonen, D.K. Rangel Guerrero,
J.L. Csicsvari, PLoS One 11 (2016).
date_created: 2018-12-11T11:51:06Z
date_published: 2016-10-19T00:00:00Z
date_updated: 2021-01-12T06:49:35Z
day: '19'
ddc:
- '570'
- '571'
department:
- _id: JoCs
doi: 10.1371/journal.pone.0164675
ec_funded: 1
file:
- access_level: open_access
checksum: 395895ecb2216e9c39135abaa56b28b3
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:13:26Z
date_updated: 2020-07-14T12:44:42Z
file_id: '5009'
file_name: IST-2016-690-v1+1_journal.pone.0164675.PDF
file_size: 4353592
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file_date_updated: 2020-07-14T12:44:42Z
has_accepted_license: '1'
intvolume: ' 11'
issue: '10'
language:
- iso: eng
month: '10'
oa: 1
oa_version: Published Version
project:
- _id: 25681D80-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '291734'
name: International IST Postdoc Fellowship Programme
- _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: PLoS One
publication_status: published
publisher: Public Library of Science
publist_id: '6037'
pubrep_id: '690'
quality_controlled: '1'
scopus_import: 1
status: public
title: Optogenetically blocking sharp wave ripple events in sleep does not interfere
with the formation of stable spatial representation in the CA1 area of the hippocampus
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: 3E5EF7F0-F248-11E8-B48F-1D18A9856A87
volume: 11
year: '2016'
...