---
_id: '14656'
abstract:
- lang: eng
  text: Although much is known about how single neurons in the hippocampus represent
    an animal's position, how circuit interactions contribute to spatial coding is
    less well understood. Using a novel statistical estimator and theoretical modeling,
    both developed in the framework of maximum entropy models, we reveal highly structured
    CA1 cell-cell interactions in male rats during open field exploration. The statistics
    of these interactions depend on whether the animal is in a familiar or novel environment.
    In both conditions the circuit interactions optimize the encoding of spatial information,
    but for regimes that differ in the informativeness of their spatial inputs. This
    structure facilitates linear decodability, making the information easy to read
    out by downstream circuits. Overall, our findings suggest that the efficient coding
    hypothesis is not only applicable to individual neuron properties in the sensory
    periphery, but also to neural interactions in the central brain.
acknowledgement: M.N. was supported by the European Union Horizon 2020 Grant 665385.
  J.C. was supported by the European Research Council Consolidator Grant 281511. G.T.
  was supported by the Austrian Science Fund (FWF) Grant P34015. C.S. was supported
  by an Institute of Science and Technology fellow award and by the National Science
  Foundation (NSF) Award No. 1922658. We thank Peter Baracskay, Karola Kaefer, and
  Hugo Malagon-Vina for the acquisition of the data. We also thank Federico Stella,
  Wiktor Młynarski, Dori Derdikman, Colin Bredenberg, Roman Huszar, Heloisa Chiossi,
  Lorenzo Posani, and Mohamady El-Gaby for comments on an earlier version of the manuscript.
article_processing_charge: Yes (in subscription journal)
article_type: original
author:
- first_name: Michele
  full_name: Nardin, Michele
  id: 30BD0376-F248-11E8-B48F-1D18A9856A87
  last_name: Nardin
  orcid: 0000-0001-8849-6570
- 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: Gašper
  full_name: Tkačik, Gašper
  id: 3D494DCA-F248-11E8-B48F-1D18A9856A87
  last_name: Tkačik
  orcid: 0000-0002-6699-1455
- first_name: Cristina
  full_name: Savin, Cristina
  id: 3933349E-F248-11E8-B48F-1D18A9856A87
  last_name: Savin
citation:
  ama: Nardin M, Csicsvari JL, Tkačik G, Savin C. The structure of hippocampal CA1
    interactions optimizes spatial coding across experience. <i>The Journal of Neuroscience</i>.
    2023;43(48):8140-8156. doi:<a href="https://doi.org/10.1523/JNEUROSCI.0194-23.2023">10.1523/JNEUROSCI.0194-23.2023</a>
  apa: Nardin, M., Csicsvari, J. L., Tkačik, G., &#38; Savin, C. (2023). The structure
    of hippocampal CA1 interactions optimizes spatial coding across experience. <i>The
    Journal of Neuroscience</i>. Society of Neuroscience. <a href="https://doi.org/10.1523/JNEUROSCI.0194-23.2023">https://doi.org/10.1523/JNEUROSCI.0194-23.2023</a>
  chicago: Nardin, Michele, Jozsef L Csicsvari, Gašper Tkačik, and Cristina Savin.
    “The Structure of Hippocampal CA1 Interactions Optimizes Spatial Coding across
    Experience.” <i>The Journal of Neuroscience</i>. Society of Neuroscience, 2023.
    <a href="https://doi.org/10.1523/JNEUROSCI.0194-23.2023">https://doi.org/10.1523/JNEUROSCI.0194-23.2023</a>.
  ieee: M. Nardin, J. L. Csicsvari, G. Tkačik, and C. Savin, “The structure of hippocampal
    CA1 interactions optimizes spatial coding across experience,” <i>The Journal of
    Neuroscience</i>, vol. 43, no. 48. Society of Neuroscience, pp. 8140–8156, 2023.
  ista: Nardin M, Csicsvari JL, Tkačik G, Savin C. 2023. The structure of hippocampal
    CA1 interactions optimizes spatial coding across experience. The Journal of Neuroscience.
    43(48), 8140–8156.
  mla: Nardin, Michele, et al. “The Structure of Hippocampal CA1 Interactions Optimizes
    Spatial Coding across Experience.” <i>The Journal of Neuroscience</i>, vol. 43,
    no. 48, Society of Neuroscience, 2023, pp. 8140–56, doi:<a href="https://doi.org/10.1523/JNEUROSCI.0194-23.2023">10.1523/JNEUROSCI.0194-23.2023</a>.
  short: M. Nardin, J.L. Csicsvari, G. Tkačik, C. Savin, The Journal of Neuroscience
    43 (2023) 8140–8156.
date_created: 2023-12-10T23:00:58Z
date_published: 2023-11-29T00:00:00Z
date_updated: 2023-12-11T11:37:20Z
day: '29'
ddc:
- '570'
department:
- _id: JoCs
- _id: GaTk
doi: 10.1523/JNEUROSCI.0194-23.2023
ec_funded: 1
external_id:
  pmid:
  - '37758476'
file:
- access_level: closed
  checksum: e2503c8f84be1050e28f64320f1d5bd2
  content_type: application/pdf
  creator: dernst
  date_created: 2023-12-11T11:30:37Z
  date_updated: 2023-12-11T11:30:37Z
  embargo: 2024-06-01
  embargo_to: open_access
  file_id: '14674'
  file_name: 2023_JourNeuroscience_Nardin.pdf
  file_size: 2280632
  relation: main_file
file_date_updated: 2023-12-11T11:30:37Z
has_accepted_license: '1'
intvolume: '        43'
issue: '48'
language:
- iso: eng
license: https://creativecommons.org/licenses/by/4.0/
main_file_link:
- open_access: '1'
  url: https://doi.org/10.1523/JNEUROSCI.0194-23.2023
month: '11'
oa: 1
oa_version: Published Version
page: 8140-8156
pmid: 1
project:
- _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
- _id: 626c45b5-2b32-11ec-9570-e509828c1ba6
  grant_number: P34015
  name: Efficient coding with biophysical realism
- _id: 2564DBCA-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '665385'
  name: International IST Doctoral Program
publication: The Journal of Neuroscience
publication_identifier:
  eissn:
  - 1529-2401
publication_status: published
publisher: Society of Neuroscience
quality_controlled: '1'
scopus_import: '1'
status: public
title: The structure of hippocampal CA1 interactions optimizes spatial coding across
  experience
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: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 43
year: '2023'
...
---
_id: '13202'
abstract:
- lang: eng
  text: Phosphatidylinositol-4,5-bisphosphate (PI(4,5)P2) plays an essential role
    in neuronal activities through interaction with various proteins involved in signaling
    at membranes. However, the distribution pattern of PI(4,5)P2 and the association
    with these proteins on the neuronal cell membranes remain elusive. In this study,
    we established a method for visualizing PI(4,5)P2 by SDS-digested freeze-fracture
    replica labeling (SDS-FRL) to investigate the quantitative nanoscale distribution
    of PI(4,5)P2 in cryo-fixed brain. We demonstrate that PI(4,5)P2 forms tiny clusters
    with a mean size of ∼1000 nm2 rather than randomly distributed in cerebellar neuronal
    membranes in male C57BL/6J mice. These clusters show preferential accumulation
    in specific membrane compartments of different cell types, in particular, in Purkinje
    cell (PC) spines and granule cell (GC) presynaptic active zones. Furthermore,
    we revealed extensive association of PI(4,5)P2 with CaV2.1 and GIRK3 across different
    membrane compartments, whereas its association with mGluR1α was compartment specific.
    These results suggest that our SDS-FRL method provides valuable insights into
    the physiological functions of PI(4,5)P2 in neurons.
acknowledged_ssus:
- _id: EM-Fac
acknowledgement: This work was supported by The Institute of Science and Technology
  (IST) Austria, the European Union's Horizon 2020 Research and Innovation Program
  under the Marie Skłodowska-Curie Grant Agreement No. 793482 (to K.E.) and by the
  European Research Council (ERC) Grant Agreement No. 694539 (to R.S.). We thank Nicoleta
  Condruz (IST Austria, Klosterneuburg, Austria) for technical assistance with sample
  preparation, the Electron Microscopy Facility of IST Austria (Klosterneuburg, Austria)
  for technical support with EM works, Natalia Baranova (University of Vienna, Vienna,
  Austria) and Martin Loose (IST Austria, Klosterneuburg, Austria) for advice on liposome
  preparation, and Yugo Fukazawa (University of Fukui, Fukui, Japan) for comments.
article_processing_charge: No
article_type: original
author:
- first_name: Kohgaku
  full_name: Eguchi, Kohgaku
  id: 2B7846DC-F248-11E8-B48F-1D18A9856A87
  last_name: Eguchi
  orcid: 0000-0002-6170-2546
- first_name: Elodie
  full_name: Le Monnier, Elodie
  id: 3B59276A-F248-11E8-B48F-1D18A9856A87
  last_name: Le Monnier
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
citation:
  ama: Eguchi K, Le Monnier E, Shigemoto R. Nanoscale phosphoinositide distribution
    on cell membranes of mouse cerebellar neurons. <i>The Journal of Neuroscience</i>.
    2023;43(23):4197-4216. doi:<a href="https://doi.org/10.1523/JNEUROSCI.1514-22.2023">10.1523/JNEUROSCI.1514-22.2023</a>
  apa: Eguchi, K., Le Monnier, E., &#38; Shigemoto, R. (2023). Nanoscale phosphoinositide
    distribution on cell membranes of mouse cerebellar neurons. <i>The Journal of
    Neuroscience</i>. Society for Neuroscience. <a href="https://doi.org/10.1523/JNEUROSCI.1514-22.2023">https://doi.org/10.1523/JNEUROSCI.1514-22.2023</a>
  chicago: Eguchi, Kohgaku, Elodie Le Monnier, and Ryuichi Shigemoto. “Nanoscale Phosphoinositide
    Distribution on Cell Membranes of Mouse Cerebellar Neurons.” <i>The Journal of
    Neuroscience</i>. Society for Neuroscience, 2023. <a href="https://doi.org/10.1523/JNEUROSCI.1514-22.2023">https://doi.org/10.1523/JNEUROSCI.1514-22.2023</a>.
  ieee: K. Eguchi, E. Le Monnier, and R. Shigemoto, “Nanoscale phosphoinositide distribution
    on cell membranes of mouse cerebellar neurons,” <i>The Journal of Neuroscience</i>,
    vol. 43, no. 23. Society for Neuroscience, pp. 4197–4216, 2023.
  ista: Eguchi K, Le Monnier E, Shigemoto R. 2023. Nanoscale phosphoinositide distribution
    on cell membranes of mouse cerebellar neurons. The Journal of Neuroscience. 43(23),
    4197–4216.
  mla: Eguchi, Kohgaku, et al. “Nanoscale Phosphoinositide Distribution on Cell Membranes
    of Mouse Cerebellar Neurons.” <i>The Journal of Neuroscience</i>, vol. 43, no.
    23, Society for Neuroscience, 2023, pp. 4197–216, doi:<a href="https://doi.org/10.1523/JNEUROSCI.1514-22.2023">10.1523/JNEUROSCI.1514-22.2023</a>.
  short: K. Eguchi, E. Le Monnier, R. Shigemoto, The Journal of Neuroscience 43 (2023)
    4197–4216.
date_created: 2023-07-09T22:01:12Z
date_published: 2023-06-07T00:00:00Z
date_updated: 2023-10-18T07:12:47Z
day: '07'
ddc:
- '570'
department:
- _id: RySh
doi: 10.1523/JNEUROSCI.1514-22.2023
ec_funded: 1
external_id:
  isi:
  - '001020132100005'
  pmid:
  - '37160366'
file:
- access_level: open_access
  checksum: 70b2141870e0bf1c94fd343e18fdbc32
  content_type: application/pdf
  creator: alisjak
  date_created: 2023-07-10T09:04:58Z
  date_updated: 2023-07-10T09:04:58Z
  file_id: '13205'
  file_name: 2023_JN_Eguchi.pdf
  file_size: 7794425
  relation: main_file
  success: 1
file_date_updated: 2023-07-10T09:04:58Z
has_accepted_license: '1'
intvolume: '        43'
isi: 1
issue: '23'
language:
- iso: eng
month: '06'
oa: 1
oa_version: Published Version
page: 4197-4216
pmid: 1
project:
- _id: 2659CC84-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '793482'
  name: 'Ultrastructural analysis of phosphoinositides in nerve terminals: distribution,
    dynamics and physiological roles in synaptic transmission'
- _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'
publication: The Journal of Neuroscience
publication_identifier:
  eissn:
  - 1529-2401
  issn:
  - 0270-6474
publication_status: published
publisher: Society for Neuroscience
quality_controlled: '1'
scopus_import: '1'
status: public
title: Nanoscale phosphoinositide distribution on cell membranes of mouse cerebellar
  neurons
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: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 43
year: '2023'
...
---
_id: '9073'
abstract:
- lang: eng
  text: The sensory and cognitive abilities of the mammalian neocortex are underpinned
    by intricate columnar and laminar circuits formed from an array of diverse neuronal
    populations. One approach to determining how interactions between these circuit
    components give rise to complex behavior is to investigate the rules by which
    cortical circuits are formed and acquire functionality during development. This
    review summarizes recent research on the development of the neocortex, from genetic
    determination in neural stem cells through to the dynamic role that specific neuronal
    populations play in the earliest circuits of neocortex, and how they contribute
    to emergent function and cognition. While many of these endeavors take advantage
    of model systems, consideration will also be given to advances in our understanding
    of activity in nascent human circuits. Such cross-species perspective is imperative
    when investigating the mechanisms underlying the dysfunction of early neocortical
    circuits in neurodevelopmental disorders, so that one can identify targets amenable
    to therapeutic intervention.
acknowledgement: Work in the I.L.H.-O. laboratory was supported by European Research
  Council Grant ERC-2015-CoG 681577 and German Research Foundation Ha 4466/10-1, Ha4466/11-1,
  Ha4466/12-1, SPP 1665, and SFB 936B5. Work in the S.J.B.B. laboratory was supported
  by Biotechnology and Biological Sciences Research Council BB/P003796/1, Medical
  Research Council MR/K004387/1 and MR/T033320/1, Wellcome Trust 215199/Z/19/Z and
  102386/Z/13/Z, and John Fell Fund. Work in the S.H. laboratory was supported by
  European Research Council Grants ERC-2016-CoG 725780 LinPro and FWF SFB F78. This
  work was supported by National Institutes of Health Grant NIMH 1R01MH110553 to N.V.D.M.G.
  Work in the J.A.C. laboratory was supported by the Ludwig Family Foundation, Simons
  Foundation SFARI Research Award, and National Institutes of Health/National Institute
  of Mental Health R01 MH102365 and R01MH113852. The B.V. laboratory was supported
  by Whitehall Foundation 2017-12-73, National Science Foundation 1736028, National
  Institutes of Health, National Institute of General Medical Sciences R01GM134363-01,
  and Halıcıoğlu Data Science Institute Fellowship. This work was supported by the
  University of California San Diego School of Medicine.
article_processing_charge: No
article_type: original
author:
- first_name: Ileana L.
  full_name: Hanganu-Opatz, Ileana L.
  last_name: Hanganu-Opatz
- first_name: Simon J. B.
  full_name: Butt, Simon J. B.
  last_name: Butt
- first_name: Simon
  full_name: Hippenmeyer, Simon
  id: 37B36620-F248-11E8-B48F-1D18A9856A87
  last_name: Hippenmeyer
  orcid: 0000-0003-2279-1061
- first_name: Natalia V.
  full_name: De Marco García, Natalia V.
  last_name: De Marco García
- first_name: Jessica A.
  full_name: Cardin, Jessica A.
  last_name: Cardin
- first_name: Bradley
  full_name: Voytek, Bradley
  last_name: Voytek
- first_name: Alysson R.
  full_name: Muotri, Alysson R.
  last_name: Muotri
citation:
  ama: Hanganu-Opatz IL, Butt SJB, Hippenmeyer S, et al. The logic of developing neocortical
    circuits in health and disease. <i>The Journal of Neuroscience</i>. 2021;41(5):813-822.
    doi:<a href="https://doi.org/10.1523/jneurosci.1655-20.2020">10.1523/jneurosci.1655-20.2020</a>
  apa: Hanganu-Opatz, I. L., Butt, S. J. B., Hippenmeyer, S., De Marco García, N.
    V., Cardin, J. A., Voytek, B., &#38; Muotri, A. R. (2021). The logic of developing
    neocortical circuits in health and disease. <i>The Journal of Neuroscience</i>.
    Society for Neuroscience. <a href="https://doi.org/10.1523/jneurosci.1655-20.2020">https://doi.org/10.1523/jneurosci.1655-20.2020</a>
  chicago: Hanganu-Opatz, Ileana L., Simon J. B. Butt, Simon Hippenmeyer, Natalia
    V. De Marco García, Jessica A. Cardin, Bradley Voytek, and Alysson R. Muotri.
    “The Logic of Developing Neocortical Circuits in Health and Disease.” <i>The Journal
    of Neuroscience</i>. Society for Neuroscience, 2021. <a href="https://doi.org/10.1523/jneurosci.1655-20.2020">https://doi.org/10.1523/jneurosci.1655-20.2020</a>.
  ieee: I. L. Hanganu-Opatz <i>et al.</i>, “The logic of developing neocortical circuits
    in health and disease,” <i>The Journal of Neuroscience</i>, vol. 41, no. 5. Society
    for Neuroscience, pp. 813–822, 2021.
  ista: Hanganu-Opatz IL, Butt SJB, Hippenmeyer S, De Marco García NV, Cardin JA,
    Voytek B, Muotri AR. 2021. The logic of developing neocortical circuits in health
    and disease. The Journal of Neuroscience. 41(5), 813–822.
  mla: Hanganu-Opatz, Ileana L., et al. “The Logic of Developing Neocortical Circuits
    in Health and Disease.” <i>The Journal of Neuroscience</i>, vol. 41, no. 5, Society
    for Neuroscience, 2021, pp. 813–22, doi:<a href="https://doi.org/10.1523/jneurosci.1655-20.2020">10.1523/jneurosci.1655-20.2020</a>.
  short: I.L. Hanganu-Opatz, S.J.B. Butt, S. Hippenmeyer, N.V. De Marco García, J.A.
    Cardin, B. Voytek, A.R. Muotri, The Journal of Neuroscience 41 (2021) 813–822.
date_created: 2021-02-03T12:23:51Z
date_published: 2021-02-03T00:00:00Z
date_updated: 2023-09-05T14:03:17Z
day: '03'
ddc:
- '570'
department:
- _id: SiHi
doi: 10.1523/jneurosci.1655-20.2020
ec_funded: 1
external_id:
  isi:
  - '000616763400002'
  pmid:
  - '33431633'
file:
- access_level: open_access
  checksum: 578fd7ed1a0aef74bce61bea2d987b33
  content_type: application/pdf
  creator: dernst
  date_created: 2022-05-27T06:59:55Z
  date_updated: 2022-05-27T06:59:55Z
  file_id: '11414'
  file_name: 2021_JourNeuroscience_Hanganu.pdf
  file_size: 1031150
  relation: main_file
  success: 1
file_date_updated: 2022-05-27T06:59:55Z
has_accepted_license: '1'
intvolume: '        41'
isi: 1
issue: '5'
keyword:
- General Neuroscience
language:
- iso: eng
month: '02'
oa: 1
oa_version: Published Version
page: 813-822
pmid: 1
project:
- _id: 260018B0-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '725780'
  name: Principles of Neural Stem Cell Lineage Progression in Cerebral Cortex Development
- _id: 059F6AB4-7A3F-11EA-A408-12923DDC885E
  grant_number: F07805
  name: Molecular Mechanisms of Neural Stem Cell Lineage Progression
publication: The Journal of Neuroscience
publication_identifier:
  eissn:
  - 1529-2401
  issn:
  - 0270-6474
publication_status: published
publisher: Society for Neuroscience
quality_controlled: '1'
scopus_import: '1'
status: public
title: The logic of developing neocortical circuits in health and disease
type: journal_article
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 41
year: '2021'
...
---
_id: '10051'
abstract:
- lang: eng
  text: 'Rab-interacting molecule (RIM)-binding protein 2 (BP2) is a multidomain protein
    of the presynaptic active zone (AZ). By binding to RIM, bassoon (Bsn), and voltage-gated
    Ca2+ channels (CaV), it is considered to be a central organizer of the topography
    of CaV and release sites of synaptic vesicles (SVs) at the AZ. Here, we used RIM-BP2
    knock-out (KO) mice and their wild-type (WT) littermates of either sex to investigate
    the role of RIM-BP2 at the endbulb of Held synapse of auditory nerve fibers (ANFs)
    with bushy cells (BCs) of the cochlear nucleus, a fast relay of the auditory pathway
    with high release probability. Disruption of RIM-BP2 lowered release probability
    altering short-term plasticity and reduced evoked EPSCs. Analysis of SV pool dynamics
    during high-frequency train stimulation indicated a reduction of SVs with high
    release probability but an overall normal size of the readily releasable SV pool
    (RRP). The Ca2+-dependent fast component of SV replenishment after RRP depletion
    was slowed. Ultrastructural analysis by superresolution light and electron microscopy
    revealed an impaired topography of presynaptic CaV and a reduction of docked and
    membrane-proximal SVs at the AZ. We conclude that RIM-BP2 organizes the topography
    of CaV, and promotes SV tethering and docking. This way RIM-BP2 is critical for
    establishing a high initial release probability as required to reliably signal
    sound onset information that we found to be degraded in BCs of RIM-BP2-deficient
    mice in vivo. SIGNIFICANCE STATEMENT: Rab-interacting molecule (RIM)-binding proteins
    (BPs) are key organizers of the active zone (AZ). Using a multidisciplinary approach
    to the calyceal endbulb of Held synapse that transmits auditory information at
    rates of up to hundreds of Hertz with submillisecond precision we demonstrate
    a requirement for RIM-BP2 for normal auditory signaling. Endbulb synapses lacking
    RIM-BP2 show a reduced release probability despite normal whole-terminal Ca2+
    influx and abundance of the key priming protein Munc13-1, a reduced rate of SV
    replenishment, as well as an altered topography of voltage-gated (CaV)2.1 Ca2+
    channels, and fewer docked and membrane proximal synaptic vesicles (SVs). This
    hampers transmission of sound onset information likely affecting downstream neural
    computations such as of sound localization.'
acknowledgement: This work was supported by the Deutsche Forschungsgemeinschaft (DFG,
  German Research Foundation) through the Collaborative Sensory Research Center 1286
  [to C.W. (A4) and T.M. (B5)] and under Germany’s Excellence Strategy Grant EXC 2067/1-390729940.
  We thank S. Gerke, A.J. Goldak, and C. Senger-Freitag for expert technical assistance;
  G. Hoch for developing image analysis routines; and S. Chepurwar and N. Strenzke
  for technical support and discussion regarding in vivo experiments. We also thank
  Dr. Christian Rosenmund, Dr. Katharina Grauel, and Dr. Stephan Sigrist for providing
  RIM-BP2 KO mice and Dr. Masahiko Watanabe for providing the anti-neurexin-antibody,
  and Dr. Toshihisa Ohtsuka for the anti-ELKS-antibody. J. Neef for help with the
  STED imaging and image analysis; E. Neher and S. Rizzoli for discussion and comments
  on the manuscript; K. Eguchi for help with the statistical analysis; and C. H. Huang
  and J. Neef for constant support and scientific discussion.
article_processing_charge: No
article_type: original
author:
- first_name: Tanvi
  full_name: Butola, Tanvi
  last_name: Butola
- first_name: Theocharis
  full_name: Alvanos, Theocharis
  last_name: Alvanos
- first_name: Anika
  full_name: Hintze, Anika
  last_name: Hintze
- first_name: Peter
  full_name: Koppensteiner, Peter
  id: 3B8B25A8-F248-11E8-B48F-1D18A9856A87
  last_name: Koppensteiner
  orcid: 0000-0002-3509-1948
- first_name: David
  full_name: Kleindienst, David
  id: 42E121A4-F248-11E8-B48F-1D18A9856A87
  last_name: Kleindienst
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
- first_name: Carolin
  full_name: Wichmann, Carolin
  last_name: Wichmann
- first_name: Tobias
  full_name: Moser, Tobias
  last_name: Moser
citation:
  ama: Butola T, Alvanos T, Hintze A, et al. RIM-binding protein 2 organizes Ca<sup>21</sup>
    channel topography and regulates release probability and vesicle replenishment
    at a fast central synapse. <i>Journal of Neuroscience</i>. 2021;41(37):7742-7767.
    doi:<a href="https://doi.org/10.1523/JNEUROSCI.0586-21.2021">10.1523/JNEUROSCI.0586-21.2021</a>
  apa: Butola, T., Alvanos, T., Hintze, A., Koppensteiner, P., Kleindienst, D., Shigemoto,
    R., … Moser, T. (2021). RIM-binding protein 2 organizes Ca<sup>21</sup> channel
    topography and regulates release probability and vesicle replenishment at a fast
    central synapse. <i>Journal of Neuroscience</i>. Society for Neuroscience. <a
    href="https://doi.org/10.1523/JNEUROSCI.0586-21.2021">https://doi.org/10.1523/JNEUROSCI.0586-21.2021</a>
  chicago: Butola, Tanvi, Theocharis Alvanos, Anika Hintze, Peter Koppensteiner, David
    Kleindienst, Ryuichi Shigemoto, Carolin Wichmann, and Tobias Moser. “RIM-Binding
    Protein 2 Organizes Ca<sup>21</sup> Channel Topography and Regulates Release Probability
    and Vesicle Replenishment at a Fast Central Synapse.” <i>Journal of Neuroscience</i>.
    Society for Neuroscience, 2021. <a href="https://doi.org/10.1523/JNEUROSCI.0586-21.2021">https://doi.org/10.1523/JNEUROSCI.0586-21.2021</a>.
  ieee: T. Butola <i>et al.</i>, “RIM-binding protein 2 organizes Ca<sup>21</sup>
    channel topography and regulates release probability and vesicle replenishment
    at a fast central synapse,” <i>Journal of Neuroscience</i>, vol. 41, no. 37. Society
    for Neuroscience, pp. 7742–7767, 2021.
  ista: Butola T, Alvanos T, Hintze A, Koppensteiner P, Kleindienst D, Shigemoto R,
    Wichmann C, Moser T. 2021. RIM-binding protein 2 organizes Ca<sup>21</sup> channel
    topography and regulates release probability and vesicle replenishment at a fast
    central synapse. Journal of Neuroscience. 41(37), 7742–7767.
  mla: Butola, Tanvi, et al. “RIM-Binding Protein 2 Organizes Ca<sup>21</sup> Channel
    Topography and Regulates Release Probability and Vesicle Replenishment at a Fast
    Central Synapse.” <i>Journal of Neuroscience</i>, vol. 41, no. 37, Society for
    Neuroscience, 2021, pp. 7742–67, doi:<a href="https://doi.org/10.1523/JNEUROSCI.0586-21.2021">10.1523/JNEUROSCI.0586-21.2021</a>.
  short: T. Butola, T. Alvanos, A. Hintze, P. Koppensteiner, D. Kleindienst, R. Shigemoto,
    C. Wichmann, T. Moser, Journal of Neuroscience 41 (2021) 7742–7767.
date_created: 2021-09-27T14:33:13Z
date_published: 2021-09-15T00:00:00Z
date_updated: 2023-08-14T06:56:30Z
day: '15'
ddc:
- '570'
department:
- _id: RySh
doi: 10.1523/JNEUROSCI.0586-21.2021
external_id:
  isi:
  - '000752287700005'
  pmid:
  - '34353898'
file:
- access_level: open_access
  checksum: 769ab627c7355a50ccfd445e43a5f351
  content_type: application/pdf
  creator: dernst
  date_created: 2022-05-31T09:10:15Z
  date_updated: 2022-05-31T09:10:15Z
  file_id: '11423'
  file_name: 2021_JourNeuroscience_Butola.pdf
  file_size: 11571961
  relation: main_file
  success: 1
file_date_updated: 2022-05-31T09:10:15Z
has_accepted_license: '1'
intvolume: '        41'
isi: 1
issue: '37'
language:
- iso: eng
month: '09'
oa: 1
oa_version: Published Version
page: 7742-7767
pmid: 1
publication: Journal of Neuroscience
publication_identifier:
  eissn:
  - 1529-2401
  issn:
  - 0270-6474
publication_status: published
publisher: Society for Neuroscience
quality_controlled: '1'
scopus_import: '1'
status: public
title: RIM-binding protein 2 organizes Ca<sup>21</sup> channel topography and regulates
  release probability and vesicle replenishment at a fast central synapse
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: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 41
year: '2021'
...
---
_id: '8084'
abstract:
- lang: eng
  text: Origin and functions of intermittent transitions among sleep stages, including
    brief awakenings and arousals, constitute a challenge to the current homeostatic
    framework for sleep regulation, focusing on factors modulating sleep over large
    time scales. Here we propose that the complex micro-architecture characterizing
    sleep on scales of seconds and minutes results from intrinsic non-equilibrium
    critical dynamics. We investigate θ- and δ-wave dynamics in control rats and in
    rats where the sleep-promoting ventrolateral preoptic nucleus (VLPO) is lesioned
    (male Sprague-Dawley rats). We demonstrate that bursts in θ and δ cortical rhythms
    exhibit complex temporal organization, with long-range correlations and robust
    duality of power-law (θ-bursts, active phase) and exponential-like (δ-bursts,
    quiescent phase) duration distributions, features typical of non-equilibrium systems
    self-organizing at criticality. We show that such non-equilibrium behavior relates
    to anti-correlated coupling between θ- and δ-bursts, persists across a range of
    time scales, and is independent of the dominant physiologic state; indications
    of a basic principle in sleep regulation. Further, we find that VLPO lesions lead
    to a modulation of cortical dynamics resulting in altered dynamical parameters
    of θ- and δ-bursts and significant reduction in θ–δ coupling. Our empirical findings
    and model simulations demonstrate that θ–δ coupling is essential for the emerging
    non-equilibrium critical dynamics observed across the sleep–wake cycle, and indicate
    that VLPO neurons may have dual role for both sleep and arousal/brief wake activation.
    The uncovered critical behavior in sleep- and wake-related cortical rhythms indicates
    a mechanism essential for the micro-architecture of spontaneous sleep-stage and
    arousal transitions within a novel, non-homeostatic paradigm of sleep regulation.
article_processing_charge: No
article_type: original
author:
- first_name: Fabrizio
  full_name: Lombardi, Fabrizio
  id: A057D288-3E88-11E9-986D-0CF4E5697425
  last_name: Lombardi
  orcid: 0000-0003-2623-5249
- first_name: Manuel
  full_name: Gómez-Extremera, Manuel
  last_name: Gómez-Extremera
- first_name: Pedro
  full_name: Bernaola-Galván, Pedro
  last_name: Bernaola-Galván
- first_name: Ramalingam
  full_name: Vetrivelan, Ramalingam
  last_name: Vetrivelan
- first_name: Clifford B.
  full_name: Saper, Clifford B.
  last_name: Saper
- first_name: Thomas E.
  full_name: Scammell, Thomas E.
  last_name: Scammell
- first_name: Plamen Ch.
  full_name: Ivanov, Plamen Ch.
  last_name: Ivanov
citation:
  ama: Lombardi F, Gómez-Extremera M, Bernaola-Galván P, et al. Critical dynamics
    and coupling in bursts of cortical rhythms indicate non-homeostatic mechanism
    for sleep-stage transitions and dual role of VLPO neurons in both sleep and wake.
    <i>Journal of Neuroscience</i>. 2020;40(1):171-190. doi:<a href="https://doi.org/10.1523/jneurosci.1278-19.2019">10.1523/jneurosci.1278-19.2019</a>
  apa: Lombardi, F., Gómez-Extremera, M., Bernaola-Galván, P., Vetrivelan, R., Saper,
    C. B., Scammell, T. E., &#38; Ivanov, P. C. (2020). Critical dynamics and coupling
    in bursts of cortical rhythms indicate non-homeostatic mechanism for sleep-stage
    transitions and dual role of VLPO neurons in both sleep and wake. <i>Journal of
    Neuroscience</i>. Society for Neuroscience. <a href="https://doi.org/10.1523/jneurosci.1278-19.2019">https://doi.org/10.1523/jneurosci.1278-19.2019</a>
  chicago: Lombardi, Fabrizio, Manuel Gómez-Extremera, Pedro Bernaola-Galván, Ramalingam
    Vetrivelan, Clifford B. Saper, Thomas E. Scammell, and Plamen Ch. Ivanov. “Critical
    Dynamics and Coupling in Bursts of Cortical Rhythms Indicate Non-Homeostatic Mechanism
    for Sleep-Stage Transitions and Dual Role of VLPO Neurons in Both Sleep and Wake.”
    <i>Journal of Neuroscience</i>. Society for Neuroscience, 2020. <a href="https://doi.org/10.1523/jneurosci.1278-19.2019">https://doi.org/10.1523/jneurosci.1278-19.2019</a>.
  ieee: F. Lombardi <i>et al.</i>, “Critical dynamics and coupling in bursts of cortical
    rhythms indicate non-homeostatic mechanism for sleep-stage transitions and dual
    role of VLPO neurons in both sleep and wake,” <i>Journal of Neuroscience</i>,
    vol. 40, no. 1. Society for Neuroscience, pp. 171–190, 2020.
  ista: Lombardi F, Gómez-Extremera M, Bernaola-Galván P, Vetrivelan R, Saper CB,
    Scammell TE, Ivanov PC. 2020. Critical dynamics and coupling in bursts of cortical
    rhythms indicate non-homeostatic mechanism for sleep-stage transitions and dual
    role of VLPO neurons in both sleep and wake. Journal of Neuroscience. 40(1), 171–190.
  mla: Lombardi, Fabrizio, et al. “Critical Dynamics and Coupling in Bursts of Cortical
    Rhythms Indicate Non-Homeostatic Mechanism for Sleep-Stage Transitions and Dual
    Role of VLPO Neurons in Both Sleep and Wake.” <i>Journal of Neuroscience</i>,
    vol. 40, no. 1, Society for Neuroscience, 2020, pp. 171–90, doi:<a href="https://doi.org/10.1523/jneurosci.1278-19.2019">10.1523/jneurosci.1278-19.2019</a>.
  short: F. Lombardi, M. Gómez-Extremera, P. Bernaola-Galván, R. Vetrivelan, C.B.
    Saper, T.E. Scammell, P.C. Ivanov, Journal of Neuroscience 40 (2020) 171–190.
date_created: 2020-07-05T15:24:51Z
date_published: 2020-01-02T00:00:00Z
date_updated: 2023-09-05T14:02:55Z
day: '02'
ddc:
- '570'
department:
- _id: GaTk
doi: 10.1523/jneurosci.1278-19.2019
ec_funded: 1
external_id:
  isi:
  - '000505167600016'
  pmid:
  - '31694962'
file:
- access_level: open_access
  content_type: application/pdf
  creator: dernst
  date_created: 2020-07-22T11:44:48Z
  date_updated: 2020-07-22T11:44:48Z
  file_id: '8150'
  file_name: 2020_JournNeuroscience_Lombardi.pdf
  file_size: 6646046
  relation: main_file
  success: 1
file_date_updated: 2020-07-22T11:44:48Z
has_accepted_license: '1'
intvolume: '        40'
isi: 1
issue: '1'
language:
- iso: eng
month: '01'
oa: 1
oa_version: Published Version
page: 171-190
pmid: 1
project:
- _id: 260C2330-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '754411'
  name: ISTplus - Postdoctoral Fellowships
publication: Journal of Neuroscience
publication_identifier:
  eissn:
  - 1529-2401
  issn:
  - 0270-6474
publication_status: published
publisher: Society for Neuroscience
quality_controlled: '1'
scopus_import: '1'
status: public
title: Critical dynamics and coupling in bursts of cortical rhythms indicate non-homeostatic
  mechanism for sleep-stage transitions and dual role of VLPO neurons in both sleep
  and wake
type: journal_article
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 40
year: '2020'
...
---
_id: '8126'
abstract:
- lang: eng
  text: Cortical areas comprise multiple types of inhibitory interneurons with stereotypical
    connectivity motifs, but their combined effect on postsynaptic dynamics has been
    largely unexplored. Here, we analyse the response of a single postsynaptic model
    neuron receiving tuned excitatory connections alongside inhibition from two plastic
    populations. Depending on the inhibitory plasticity rule, synapses remain unspecific
    (flat), become anti-correlated to, or mirror excitatory synapses. Crucially, the
    neuron’s receptive field, i.e., its response to presynaptic stimuli, depends on
    the modulatory state of inhibition. When both inhibitory populations are active,
    inhibition balances excitation, resulting in uncorrelated postsynaptic responses
    regardless of the inhibitory tuning profiles. Modulating the activity of a given
    inhibitory population produces strong correlations to either preferred or non-preferred
    inputs, in line with recent experimental findings showing dramatic context-dependent
    changes of neurons’ receptive fields. We thus confirm that a neuron’s receptive
    field doesn’t follow directly from the weight profiles of its presynaptic afferents.
article_processing_charge: No
article_type: original
author:
- first_name: Everton J.
  full_name: Agnes, Everton J.
  last_name: Agnes
  orcid: 0000-0001-7184-7311
- first_name: Andrea I.
  full_name: Luppi, Andrea I.
  last_name: Luppi
- first_name: Tim P
  full_name: Vogels, Tim P
  id: CB6FF8D2-008F-11EA-8E08-2637E6697425
  last_name: Vogels
  orcid: 0000-0003-3295-6181
citation:
  ama: Agnes EJ, Luppi AI, Vogels TP. Complementary inhibitory weight profiles emerge
    from plasticity and allow attentional switching of receptive fields. <i>The Journal
    of Neuroscience</i>. 2020;40(50):9634-9649. doi:<a href="https://doi.org/10.1523/JNEUROSCI.0276-20.2020">10.1523/JNEUROSCI.0276-20.2020</a>
  apa: Agnes, E. J., Luppi, A. I., &#38; Vogels, T. P. (2020). Complementary inhibitory
    weight profiles emerge from plasticity and allow attentional switching of receptive
    fields. <i>The Journal of Neuroscience</i>. Society for Neuroscience. <a href="https://doi.org/10.1523/JNEUROSCI.0276-20.2020">https://doi.org/10.1523/JNEUROSCI.0276-20.2020</a>
  chicago: Agnes, Everton J., Andrea I. Luppi, and Tim P Vogels. “Complementary Inhibitory
    Weight Profiles Emerge from Plasticity and Allow Attentional Switching of Receptive
    Fields.” <i>The Journal of Neuroscience</i>. Society for Neuroscience, 2020. <a
    href="https://doi.org/10.1523/JNEUROSCI.0276-20.2020">https://doi.org/10.1523/JNEUROSCI.0276-20.2020</a>.
  ieee: E. J. Agnes, A. I. Luppi, and T. P. Vogels, “Complementary inhibitory weight
    profiles emerge from plasticity and allow attentional switching of receptive fields,”
    <i>The Journal of Neuroscience</i>, vol. 40, no. 50. Society for Neuroscience,
    pp. 9634–9649, 2020.
  ista: Agnes EJ, Luppi AI, Vogels TP. 2020. Complementary inhibitory weight profiles
    emerge from plasticity and allow attentional switching of receptive fields. The
    Journal of Neuroscience. 40(50), 9634–9649.
  mla: Agnes, Everton J., et al. “Complementary Inhibitory Weight Profiles Emerge
    from Plasticity and Allow Attentional Switching of Receptive Fields.” <i>The Journal
    of Neuroscience</i>, vol. 40, no. 50, Society for Neuroscience, 2020, pp. 9634–49,
    doi:<a href="https://doi.org/10.1523/JNEUROSCI.0276-20.2020">10.1523/JNEUROSCI.0276-20.2020</a>.
  short: E.J. Agnes, A.I. Luppi, T.P. Vogels, The Journal of Neuroscience 40 (2020)
    9634–9649.
date_created: 2020-07-16T12:25:04Z
date_published: 2020-12-09T00:00:00Z
date_updated: 2023-08-22T07:54:26Z
day: '09'
ddc:
- '570'
department:
- _id: TiVo
doi: 10.1523/JNEUROSCI.0276-20.2020
external_id:
  isi:
  - '000606706400009'
  pmid:
  - '33168622'
file:
- access_level: open_access
  checksum: 7977e4dd6b89357d1a5cc88babac56da
  content_type: application/pdf
  creator: dernst
  date_created: 2020-12-28T08:31:47Z
  date_updated: 2020-12-28T08:31:47Z
  file_id: '8977'
  file_name: 2020_JourNeuroscience_Agnes.pdf
  file_size: 2750920
  relation: main_file
  success: 1
file_date_updated: 2020-12-28T08:31:47Z
has_accepted_license: '1'
intvolume: '        40'
isi: 1
issue: '50'
language:
- iso: eng
month: '12'
oa: 1
oa_version: Published Version
page: 9634-9649
pmid: 1
publication: The Journal of Neuroscience
publication_identifier:
  eissn:
  - 1529-2401
publication_status: published
publisher: Society for Neuroscience
quality_controlled: '1'
scopus_import: '1'
status: public
title: Complementary inhibitory weight profiles emerge from plasticity and allow attentional
  switching of receptive fields
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: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 40
year: '2020'
...
---
_id: '2018'
abstract:
- lang: eng
  text: Synaptic cell adhesion molecules are increasingly gaining attention for conferring
    specific properties to individual synapses. Netrin-G1 and netrin-G2 are trans-synaptic
    adhesion molecules that distribute on distinct axons, and their presence restricts
    the expression of their cognate receptors, NGL1 and NGL2, respectively, to specific
    subdendritic segments of target neurons. However, the neural circuits and functional
    roles of netrin-G isoform complexes remain unclear. Here, we use netrin-G-KO and
    NGL-KO mice to reveal that netrin-G1/NGL1 and netrin-G2/NGL2 interactions specify
    excitatory synapses in independent hippocampal pathways. In the hippocampal CA1
    area, netrin-G1/NGL1 and netrin-G2/NGL2 were expressed in the temporoammonic and
    Schaffer collateral pathways, respectively. The lack of presynaptic netrin-Gs
    led to the dispersion of NGLs from postsynaptic membranes. In accord, netrin-G
    mutant synapses displayed opposing phenotypes in long-term and short-term plasticity
    through discrete biochemical pathways. The plasticity phenotypes in netrin-G-KOs
    were phenocopied in NGL-KOs, with a corresponding loss of netrin-Gs from presynaptic
    membranes. Our findings show that netrin-G/NGL interactions differentially control
    synaptic plasticity in distinct circuits via retrograde signaling mechanisms and
    explain how synaptic inputs are diversified to control neuronal activity.
acknowledgement: This work was supported by “Funding Program for World-Leading Innovative
  R&D on Science and Technology (FIRST Program)” initiated by the Council for Science
  and Technology Policy.
article_processing_charge: No
article_type: original
author:
- first_name: Hiroshi
  full_name: Matsukawa, Hiroshi
  last_name: Matsukawa
- first_name: Sachiko
  full_name: Akiyoshi Nishimura, Sachiko
  last_name: Akiyoshi Nishimura
- first_name: Qi
  full_name: Zhang, Qi
  last_name: Zhang
- first_name: Rafael
  full_name: Luján, Rafael
  last_name: Luján
- first_name: Kazuhiko
  full_name: Yamaguchi, Kazuhiko
  last_name: Yamaguchi
- first_name: Hiromichi
  full_name: Goto, Hiromichi
  last_name: Goto
- first_name: Kunio
  full_name: Yaguchi, Kunio
  last_name: Yaguchi
- first_name: Tsutomu
  full_name: Hashikawa, Tsutomu
  last_name: Hashikawa
- first_name: Chie
  full_name: Sano, Chie
  last_name: Sano
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
- first_name: Toshiaki
  full_name: Nakashiba, Toshiaki
  last_name: Nakashiba
- first_name: Shigeyoshi
  full_name: Itohara, Shigeyoshi
  last_name: Itohara
citation:
  ama: Matsukawa H, Akiyoshi Nishimura S, Zhang Q, et al. Netrin-G/NGL complexes encode
    functional synaptic diversification. <i>Journal of Neuroscience</i>. 2014;34(47):15779-15792.
    doi:<a href="https://doi.org/10.1523/JNEUROSCI.1141-14.2014">10.1523/JNEUROSCI.1141-14.2014</a>
  apa: Matsukawa, H., Akiyoshi Nishimura, S., Zhang, Q., Luján, R., Yamaguchi, K.,
    Goto, H., … Itohara, S. (2014). Netrin-G/NGL complexes encode functional synaptic
    diversification. <i>Journal of Neuroscience</i>. Society for Neuroscience. <a
    href="https://doi.org/10.1523/JNEUROSCI.1141-14.2014">https://doi.org/10.1523/JNEUROSCI.1141-14.2014</a>
  chicago: Matsukawa, Hiroshi, Sachiko Akiyoshi Nishimura, Qi Zhang, Rafael Luján,
    Kazuhiko Yamaguchi, Hiromichi Goto, Kunio Yaguchi, et al. “Netrin-G/NGL Complexes
    Encode Functional Synaptic Diversification.” <i>Journal of Neuroscience</i>. Society
    for Neuroscience, 2014. <a href="https://doi.org/10.1523/JNEUROSCI.1141-14.2014">https://doi.org/10.1523/JNEUROSCI.1141-14.2014</a>.
  ieee: H. Matsukawa <i>et al.</i>, “Netrin-G/NGL complexes encode functional synaptic
    diversification,” <i>Journal of Neuroscience</i>, vol. 34, no. 47. Society for
    Neuroscience, pp. 15779–15792, 2014.
  ista: Matsukawa H, Akiyoshi Nishimura S, Zhang Q, Luján R, Yamaguchi K, Goto H,
    Yaguchi K, Hashikawa T, Sano C, Shigemoto R, Nakashiba T, Itohara S. 2014. Netrin-G/NGL
    complexes encode functional synaptic diversification. Journal of Neuroscience.
    34(47), 15779–15792.
  mla: Matsukawa, Hiroshi, et al. “Netrin-G/NGL Complexes Encode Functional Synaptic
    Diversification.” <i>Journal of Neuroscience</i>, vol. 34, no. 47, Society for
    Neuroscience, 2014, pp. 15779–92, doi:<a href="https://doi.org/10.1523/JNEUROSCI.1141-14.2014">10.1523/JNEUROSCI.1141-14.2014</a>.
  short: H. Matsukawa, S. Akiyoshi Nishimura, Q. Zhang, R. Luján, K. Yamaguchi, H.
    Goto, K. Yaguchi, T. Hashikawa, C. Sano, R. Shigemoto, T. Nakashiba, S. Itohara,
    Journal of Neuroscience 34 (2014) 15779–15792.
date_created: 2018-12-11T11:55:14Z
date_published: 2014-11-19T00:00:00Z
date_updated: 2022-05-24T08:54:54Z
day: '19'
ddc:
- '570'
department:
- _id: RySh
doi: 10.1523/JNEUROSCI.1141-14.2014
external_id:
  pmid:
  - '25411505'
file:
- access_level: open_access
  checksum: 6913e9bc26e9fc1c0441a739a4199229
  content_type: application/pdf
  creator: dernst
  date_created: 2022-05-24T08:41:41Z
  date_updated: 2022-05-24T08:41:41Z
  file_id: '11410'
  file_name: 2014_JournNeuroscience_Matsukawa.pdf
  file_size: 3963728
  relation: main_file
  success: 1
file_date_updated: 2022-05-24T08:41:41Z
has_accepted_license: '1'
intvolume: '        34'
issue: '47'
language:
- iso: eng
month: '11'
oa: 1
oa_version: Published Version
page: 15779 - 15792
pmid: 1
publication: Journal of Neuroscience
publication_identifier:
  eissn:
  - 1529-2401
  issn:
  - 0270-6474
publication_status: published
publisher: Society for Neuroscience
publist_id: '5054'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Netrin-G/NGL complexes encode functional synaptic diversification
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 34
year: '2014'
...
