---
OA_place: publisher
_id: '19271'
abstract:
- lang: eng
  text: "The medial habenula (MHb) is implicated in regulating emotional responses\r\nto
    aversive events. Studies in zebrafish have identified a remarkable morphological\r\nleft-right
    asymmetry in the dorsal habenula (zebrafish equivalent of mammalian\r\nMHb)-to-interpeduncular
    nucleus (IPN) pathway and its left-side specific role in\r\nmodulating fear responses.
    However, there is little evidence for structural or\r\nfunctional lateralization
    in the mammalian MHb-IPN pathway.\r\nHere, I investigated the synaptic properties
    of the left and right MHb\r\nafferents to the IPN in mice and addressed whether
    these synaptic connections\r\nselectively influence the expression of conditioned
    fear in mice. My findings reveal\r\nthat each individual IPN neuron receives inputs
    from both left and right MHb.\r\nElectrophysiological recordings from the same
    postsynaptic IPN neurons\r\ndemonstrate that the left MHb-originating synapses
    exhibit lower release\r\nprobability and higher \U0001D6FE-aminobutyric acid type
    B receptor (GABABR)-mediated\r\npotentiation compared to the right MHb-originating
    synapses. Interestingly,\r\nchemogenetic inhibition of cholinergic neurons in
    the left but not the right MHb\r\nsignificantly attenuated cue-dependent fear
    recall. Furthermore, conditional\r\ndeletion of GABABR in the left MHb interfered
    with the recall of cued fear memory,\r\nwhereas that in the right MHb neurons
    spared fear memory expression.\r\nCollectively, I demonstrate a functional asymmetry
    of the MHb in mice,\r\nrevealing a predominant role for GABABR-mediated signaling
    in the left MHb-IPN\r\npathway in the modulation of fear memories. These findings
    suggest that\r\nlateralized pathways could represent a fundamental principle in
    the neural\r\nregulation of emotion across species."
acknowledged_ssus:
- _id: PreCl
- _id: M-Shop
acknowledgement: "I would like to thank the European Research Council and European
  Commission, under the European Union’s Horizon 2020 research and innovation program
  (ERC grant agreement no. 694539 to Ryuichi Shigemoto and the Marie Skłodowska-Curie
  grant agreement no. 665385 to Cihan Önal), and the Austrian Neuroscience Association
  for providing financial support and opportunities, which were important in allowing
  me to present my work. I also wish to thank the\r\nPreclinical Facility, especially
  Michael Schunn, for always welcoming me from my earliest days as an intern. My gratitude
  goes as well to the Miba Machine Shop, in particular Todor Asenov, Astrit Arslani,
  and Thomas Menner, whose technical expertise often saved the day."
alternative_title:
- ISTA Thesis
article_processing_charge: No
author:
- first_name: Hüseyin C
  full_name: Önal, Hüseyin C
  id: 4659D740-F248-11E8-B48F-1D18A9856A87
  last_name: Önal
  orcid: 0000-0002-2771-2011
citation:
  ama: Önal C. Asymmetrical modulation of fear expression via GABAB receptors in the
    mouse medial habenula. 2025. doi:<a href="https://doi.org/10.15479/AT-ISTA-19271">10.15479/AT-ISTA-19271</a>
  apa: Önal, C. (2025). <i>Asymmetrical modulation of fear expression via GABAB receptors
    in the mouse medial habenula</i>. Institute of Science and Technology Austria.
    <a href="https://doi.org/10.15479/AT-ISTA-19271">https://doi.org/10.15479/AT-ISTA-19271</a>
  chicago: Önal, Cihan. “Asymmetrical Modulation of Fear Expression via GABAB Receptors
    in the Mouse Medial Habenula.” Institute of Science and Technology Austria, 2025.
    <a href="https://doi.org/10.15479/AT-ISTA-19271">https://doi.org/10.15479/AT-ISTA-19271</a>.
  ieee: C. Önal, “Asymmetrical modulation of fear expression via GABAB receptors in
    the mouse medial habenula,” Institute of Science and Technology Austria, 2025.
  ista: Önal C. 2025. Asymmetrical modulation of fear expression via GABAB receptors
    in the mouse medial habenula. Institute of Science and Technology Austria.
  mla: Önal, Cihan. <i>Asymmetrical Modulation of Fear Expression via GABAB Receptors
    in the Mouse Medial Habenula</i>. Institute of Science and Technology Austria,
    2025, doi:<a href="https://doi.org/10.15479/AT-ISTA-19271">10.15479/AT-ISTA-19271</a>.
  short: C. Önal, Asymmetrical Modulation of Fear Expression via GABAB Receptors in
    the Mouse Medial Habenula, Institute of Science and Technology Austria, 2025.
corr_author: '1'
date_created: 2025-02-28T14:15:53Z
date_published: 2025-03-04T00:00:00Z
date_updated: 2026-04-07T12:40:42Z
day: '04'
ddc:
- '570'
- '571'
- '573'
- '599'
degree_awarded: PhD
department:
- _id: GradSch
- _id: RySh
doi: 10.15479/AT-ISTA-19271
ec_funded: 1
file:
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file_date_updated: 2026-02-01T23:30:02Z
has_accepted_license: '1'
language:
- iso: eng
license: https://creativecommons.org/licenses/by-nc/4.0/
month: '03'
oa: 1
oa_version: Published Version
project:
- _id: 25CA28EA-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '694539'
  name: 'In situ analysis of single channel subunit composition in neurons: physiological
    implication in synaptic plasticity and behaviour'
- _id: 2564DBCA-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '665385'
  name: International IST Doctoral Program
publication_identifier:
  eissn:
  - 2663-337X
publication_status: published
publisher: Institute of Science and Technology Austria
related_material:
  record:
  - id: '9437'
    relation: part_of_dissertation
    status: public
  - id: '15084'
    relation: part_of_dissertation
    status: public
status: public
supervisor:
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
title: Asymmetrical modulation of fear expression via GABAB receptors in the mouse
  medial habenula
tmp:
  image: /images/cc_by_nc.png
  legal_code_url: https://creativecommons.org/licenses/by-nc/4.0/legalcode
  name: Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)
  short: CC BY-NC (4.0)
type: dissertation
user_id: ba8df636-2132-11f1-aed0-ed93e2281fdd
year: '2025'
...
---
APC_amount: 5887,8 EUR
OA_place: publisher
OA_type: hybrid
_id: '15084'
abstract:
- lang: eng
  text: "GABAB receptor (GBR) activation inhibits neurotransmitter release in axon
    terminals in the brain, except in medial habenula (MHb) terminals, which show
    robust potentiation. However, mechanisms underlying this enigmatic potentiation
    remain elusive. Here, we report that GBR activation on MHb terminals induces an
    activity-dependent transition from a facilitating, tonic to a depressing, phasic
    neurotransmitter release mode. This transition is accompanied by a 4.1-fold increase
    in readily releasable vesicle pool (RRP) size and a 3.5-fold increase of docked
    synaptic vesicles (SVs) at the presynaptic active zone (AZ). Strikingly, the depressing
    phasic release exhibits looser coupling distance than the tonic release. Furthermore,
    the tonic and phasic release are selectively affected by deletion of synaptoporin
    (SPO) and Ca\r\n            <jats:sup>2+</jats:sup>\r\n            -dependent
    activator protein for secretion 2 (CAPS2), respectively. SPO modulates augmentation,
    the short-term plasticity associated with tonic release, and CAPS2 retains the
    increased RRP for initial responses in phasic response trains. The cytosolic protein
    CAPS2 showed a SV-associated distribution similar to the vesicular transmembrane
    protein SPO, and they were colocalized in the same terminals. We developed the
    “Flash and Freeze-fracture” method, and revealed the release of SPO-associated
    vesicles in both tonic and phasic modes and activity-dependent recruitment of
    CAPS2 to the AZ during phasic release, which lasted several minutes. Overall,
    these results indicate that GBR activation translocates CAPS2 to the AZ along
    with the fusion of CAPS2-associated SVs, contributing to persistency of the RRP
    increase. Thus, we identified structural and molecular mechanisms underlying tonic
    and phasic neurotransmitter release and their transition by GBR activation in
    MHb terminals."
acknowledged_ssus:
- _id: M-Shop
- _id: PreCl
- _id: EM-Fac
acknowledgement: We thank Erwin Neher and Ipe Ninan for critical comments on the manuscript.
  This project has received funding from the European Research Council (ERC) and European
  Commission, under the European Union’s Horizon 2020 research and innovation program
  (ERC grant agreement no. 694539 to R.S. and the Marie Skłodowska-Curie grant agreement
  no. 665385 to C.Ö.). This study was supported by the Cooperative Study Program of
  Center for Animal Resources and Collaborative Study of NINS. We thank Kohgaku Eguchi
  for statistical analysis, Yu Kasugai for additional EM imaging, Robert Beattie for
  the design of the slice recovery chamber for Flash and Freeze experiments, Todor
  Asenov from the ISTA machine shop for custom part preparations for high-pressure
  freezing, the ISTA preclinical facility for animal caretaking, and the ISTA EM facilities
  for technical support.
article_number: e2301449121
article_processing_charge: Yes (in subscription journal)
article_type: original
author:
- first_name: Peter
  full_name: Koppensteiner, Peter
  id: 3B8B25A8-F248-11E8-B48F-1D18A9856A87
  last_name: Koppensteiner
  orcid: 0000-0002-3509-1948
- first_name: Pradeep
  full_name: Bhandari, Pradeep
  id: 45EDD1BC-F248-11E8-B48F-1D18A9856A87
  last_name: Bhandari
  orcid: 0000-0003-0863-4481
- first_name: Hüseyin C
  full_name: Önal, Hüseyin C
  id: 4659D740-F248-11E8-B48F-1D18A9856A87
  last_name: Önal
  orcid: 0000-0002-2771-2011
- 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: Elodie
  full_name: Le Monnier, Elodie
  id: 3B59276A-F248-11E8-B48F-1D18A9856A87
  last_name: Le Monnier
- first_name: Utsa
  full_name: Roy, Utsa
  id: 4d26cf11-5355-11ee-ae5a-eb05e255b9b2
  last_name: Roy
- first_name: Yukihiro
  full_name: Nakamura, Yukihiro
  last_name: Nakamura
- first_name: Tetsushi
  full_name: Sadakata, Tetsushi
  last_name: Sadakata
- first_name: Makoto
  full_name: Sanbo, Makoto
  last_name: Sanbo
- first_name: Masumi
  full_name: Hirabayashi, Masumi
  last_name: Hirabayashi
- first_name: JeongSeop
  full_name: Rhee, JeongSeop
  last_name: Rhee
- first_name: Nils
  full_name: Brose, Nils
  last_name: Brose
- 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: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
citation:
  ama: Koppensteiner P, Bhandari P, Önal C, et al. GABAB receptors induce phasic release
    from medial habenula terminals through activity-dependent recruitment of release-ready
    vesicles. <i>Proceedings of the National Academy of Sciences of the United States
    of America</i>. 2024;121(8). doi:<a href="https://doi.org/10.1073/pnas.2301449121">10.1073/pnas.2301449121</a>
  apa: Koppensteiner, P., Bhandari, P., Önal, C., Borges Merjane, C., Le Monnier,
    E., Roy, U., … Shigemoto, R. (2024). GABAB receptors induce phasic release from
    medial habenula terminals through activity-dependent recruitment of release-ready
    vesicles. <i>Proceedings of the National Academy of Sciences of the United States
    of America</i>. National Academy of Sciences. <a href="https://doi.org/10.1073/pnas.2301449121">https://doi.org/10.1073/pnas.2301449121</a>
  chicago: Koppensteiner, Peter, Pradeep Bhandari, Cihan Önal, Carolina Borges Merjane,
    Elodie Le Monnier, Utsa Roy, Yukihiro Nakamura, et al. “GABAB Receptors Induce
    Phasic Release from Medial Habenula Terminals through Activity-Dependent Recruitment
    of Release-Ready Vesicles.” <i>Proceedings of the National Academy of Sciences
    of the United States of America</i>. National Academy of Sciences, 2024. <a href="https://doi.org/10.1073/pnas.2301449121">https://doi.org/10.1073/pnas.2301449121</a>.
  ieee: P. Koppensteiner <i>et al.</i>, “GABAB receptors induce phasic release from
    medial habenula terminals through activity-dependent recruitment of release-ready
    vesicles,” <i>Proceedings of the National Academy of Sciences of the United States
    of America</i>, vol. 121, no. 8. National Academy of Sciences, 2024.
  ista: Koppensteiner P, Bhandari P, Önal C, Borges Merjane C, Le Monnier E, Roy U,
    Nakamura Y, Sadakata T, Sanbo M, Hirabayashi M, Rhee J, Brose N, Jonas PM, Shigemoto
    R. 2024. GABAB receptors induce phasic release from medial habenula terminals
    through activity-dependent recruitment of release-ready vesicles. Proceedings
    of the National Academy of Sciences of the United States of America. 121(8), e2301449121.
  mla: Koppensteiner, Peter, et al. “GABAB Receptors Induce Phasic Release from Medial
    Habenula Terminals through Activity-Dependent Recruitment of Release-Ready Vesicles.”
    <i>Proceedings of the National Academy of Sciences of the United States of America</i>,
    vol. 121, no. 8, e2301449121, National Academy of Sciences, 2024, doi:<a href="https://doi.org/10.1073/pnas.2301449121">10.1073/pnas.2301449121</a>.
  short: P. Koppensteiner, P. Bhandari, C. Önal, C. Borges Merjane, E. Le Monnier,
    U. Roy, Y. Nakamura, T. Sadakata, M. Sanbo, M. Hirabayashi, J. Rhee, N. Brose,
    P.M. Jonas, R. Shigemoto, Proceedings of the National Academy of Sciences of the
    United States of America 121 (2024).
corr_author: '1'
date_created: 2024-03-05T09:23:55Z
date_published: 2024-02-20T00:00:00Z
date_updated: 2026-06-22T22:30:42Z
day: '20'
ddc:
- '570'
department:
- _id: RySh
- _id: PeJo
doi: 10.1073/pnas.2301449121
ec_funded: 1
external_id:
  isi:
  - '001208567300006'
  pmid:
  - '38346189'
file:
- access_level: open_access
  checksum: b25b2a057c266ff317a48b0d54d6fc8a
  content_type: application/pdf
  creator: dernst
  date_created: 2024-03-12T13:42:42Z
  date_updated: 2024-03-12T13:42:42Z
  file_id: '15110'
  file_name: 2024_PNAS_Koppensteiner.pdf
  file_size: 13648221
  relation: main_file
  success: 1
file_date_updated: 2024-03-12T13:42:42Z
has_accepted_license: '1'
intvolume: '       121'
isi: 1
issue: '8'
language:
- iso: eng
license: https://creativecommons.org/licenses/by-nc-nd/4.0/
month: '02'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: 25CA28EA-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '694539'
  name: 'In situ analysis of single channel subunit composition in neurons: physiological
    implication in synaptic plasticity and behaviour'
- _id: 2564DBCA-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '665385'
  name: International IST Doctoral Program
publication: Proceedings of the National Academy of Sciences of the United States
  of America
publication_identifier:
  eissn:
  - 1091-6490
  issn:
  - 0027-8424
publication_status: published
publisher: National Academy of Sciences
quality_controlled: '1'
related_material:
  link:
  - description: News on ISTA Website
    relation: press_release
    url: https://ista.ac.at/en/news/neuronal-insights-flash-and-freeze-fracture/
  record:
  - id: '13173'
    relation: research_data
    status: public
  - id: '19271'
    relation: dissertation_contains
    status: public
scopus_import: '1'
status: public
title: GABAB receptors induce phasic release from medial habenula terminals through
  activity-dependent recruitment of release-ready vesicles
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: 121
year: '2024'
...
---
_id: '9437'
abstract:
- lang: eng
  text: The synaptic connection from medial habenula (MHb) to interpeduncular nucleus
    (IPN) is critical for emotion-related behaviors and uniquely expresses R-type
    Ca2+ channels (Cav2.3) and auxiliary GABAB receptor (GBR) subunits, the K+-channel
    tetramerization domain-containing proteins (KCTDs). Activation of GBRs facilitates
    or inhibits transmitter release from MHb terminals depending on the IPN subnucleus,
    but the role of KCTDs is unknown. We therefore examined the localization and function
    of Cav2.3, GBRs, and KCTDs in this pathway in mice. We show in heterologous cells
    that KCTD8 and KCTD12b directly bind to Cav2.3 and that KCTD8 potentiates Cav2.3
    currents in the absence of GBRs. In the rostral IPN, KCTD8, KCTD12b, and Cav2.3
    co-localize at the presynaptic active zone. Genetic deletion indicated a bidirectional
    modulation of Cav2.3-mediated release by these KCTDs with a compensatory increase
    of KCTD8 in the active zone in KCTD12b-deficient mice. The interaction of Cav2.3
    with KCTDs therefore scales synaptic strength independent of GBR activation.
acknowledgement: We are grateful to Akari Hagiwara and Toshihisa Ohtsuka for CAST
  antibody, and Masahiko Watanabe for neurexin antibody. We thank David Adams for
  kindly providing the stable Cav2.3 cell line. Cav2.3 KO mice were kindly provided
  by Tsutomu Tanabe. This project has received funding from the European Research
  Council (ERC) and European Commission (EC), under the European Union’s Horizon 2020
  research and innovation programme (ERC grant agreement no. 694539 to Ryuichi Shigemoto,
  no. 692692 to Peter Jonas, and the Marie Skłodowska-Curie grant agreement no. 665385
  to Cihan Önal), the Swiss National Science Foundation Grant 31003A-172881 to Bernhard
  Bettler and Deutsche Forschungsgemeinschaft (For 2143) and BIOSS-2 to Akos Kulik.
article_number: e68274
article_processing_charge: No
article_type: original
author:
- first_name: Pradeep
  full_name: Bhandari, Pradeep
  id: 45EDD1BC-F248-11E8-B48F-1D18A9856A87
  last_name: Bhandari
  orcid: 0000-0003-0863-4481
- 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: Diego
  full_name: Fernández-Fernández, Diego
  last_name: Fernández-Fernández
- first_name: Thorsten
  full_name: Fritzius, Thorsten
  last_name: Fritzius
- first_name: David
  full_name: Kleindienst, David
  id: 42E121A4-F248-11E8-B48F-1D18A9856A87
  last_name: Kleindienst
- first_name: Hüseyin C
  full_name: Önal, Hüseyin C
  id: 4659D740-F248-11E8-B48F-1D18A9856A87
  last_name: Önal
  orcid: 0000-0002-2771-2011
- first_name: Jacqueline-Claire
  full_name: Montanaro-Punzengruber, Jacqueline-Claire
  id: 3786AB44-F248-11E8-B48F-1D18A9856A87
  last_name: Montanaro-Punzengruber
- first_name: Martin
  full_name: Gassmann, Martin
  last_name: Gassmann
- 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: Akos
  full_name: Kulik, Akos
  last_name: Kulik
- first_name: Bernhard
  full_name: Bettler, Bernhard
  last_name: Bettler
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
- first_name: Peter
  full_name: Koppensteiner, Peter
  id: 3B8B25A8-F248-11E8-B48F-1D18A9856A87
  last_name: Koppensteiner
  orcid: 0000-0002-3509-1948
citation:
  ama: Bhandari P, Vandael DH, Fernández-Fernández D, et al. GABAB receptor auxiliary
    subunits modulate Cav2.3-mediated release from medial habenula terminals. <i>eLife</i>.
    2021;10. doi:<a href="https://doi.org/10.7554/ELIFE.68274">10.7554/ELIFE.68274</a>
  apa: Bhandari, P., Vandael, D. H., Fernández-Fernández, D., Fritzius, T., Kleindienst,
    D., Önal, C., … Koppensteiner, P. (2021). GABAB receptor auxiliary subunits modulate
    Cav2.3-mediated release from medial habenula terminals. <i>ELife</i>. eLife Sciences
    Publications. <a href="https://doi.org/10.7554/ELIFE.68274">https://doi.org/10.7554/ELIFE.68274</a>
  chicago: Bhandari, Pradeep, David H Vandael, Diego Fernández-Fernández, Thorsten
    Fritzius, David Kleindienst, Cihan Önal, Jacqueline-Claire Montanaro-Punzengruber,
    et al. “GABAB Receptor Auxiliary Subunits Modulate Cav2.3-Mediated Release from
    Medial Habenula Terminals.” <i>ELife</i>. eLife Sciences Publications, 2021. <a
    href="https://doi.org/10.7554/ELIFE.68274">https://doi.org/10.7554/ELIFE.68274</a>.
  ieee: P. Bhandari <i>et al.</i>, “GABAB receptor auxiliary subunits modulate Cav2.3-mediated
    release from medial habenula terminals,” <i>eLife</i>, vol. 10. eLife Sciences
    Publications, 2021.
  ista: Bhandari P, Vandael DH, Fernández-Fernández D, Fritzius T, Kleindienst D,
    Önal C, Montanaro-Punzengruber J-C, Gassmann M, Jonas PM, Kulik A, Bettler B,
    Shigemoto R, Koppensteiner P. 2021. GABAB receptor auxiliary subunits modulate
    Cav2.3-mediated release from medial habenula terminals. eLife. 10, e68274.
  mla: Bhandari, Pradeep, et al. “GABAB Receptor Auxiliary Subunits Modulate Cav2.3-Mediated
    Release from Medial Habenula Terminals.” <i>ELife</i>, vol. 10, e68274, eLife
    Sciences Publications, 2021, doi:<a href="https://doi.org/10.7554/ELIFE.68274">10.7554/ELIFE.68274</a>.
  short: P. Bhandari, D.H. Vandael, D. Fernández-Fernández, T. Fritzius, D. Kleindienst,
    C. Önal, J.-C. Montanaro-Punzengruber, M. Gassmann, P.M. Jonas, A. Kulik, B. Bettler,
    R. Shigemoto, P. Koppensteiner, ELife 10 (2021).
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