Retinal horizontal cells use different synaptic sites for global feedforward and local feedback signaling.

Animals Feedback Mammals Mice Retina Retinal Cone Photoreceptor Cells Retinal Horizontal Cells / metabolism Synapses
calcium dendrite global glutamate horizontal cell local mouse neurons retina synapse

Journal

Current biology : CB
ISSN: 1879-0445
Titre abrégé: Curr Biol
Pays: England
ID NLM: 9107782

Informations de publication

Date de publication:
07 02 2022
Historique:
received: 29 10 2019
revised: 19 10 2021
accepted: 23 11 2021
pubmed: 16 12 2021
medline: 12 4 2022
entrez: 15 12 2021
Statut: ppublish

Résumé

In the outer plexiform layer (OPL) of the mammalian retina, cone photoreceptors (cones) provide input to more than a dozen types of cone bipolar cells (CBCs). In the mouse, this transmission is modulated by a single horizontal cell (HC) type. HCs perform global signaling within their laterally coupled network but also provide local, cone-specific feedback. However, it is unknown how HCs provide local feedback to cones at the same time as global forward signaling to CBCs and where the underlying synapses are located. To assess how HCs simultaneously perform different modes of signaling, we reconstructed the dendritic trees of five HCs as well as cone axon terminals and CBC dendrites in a serial block-face electron microscopy volume and analyzed their connectivity. In addition to the fine HC dendritic tips invaginating cone axon terminals, we also identified "bulbs," short segments of increased dendritic diameter on the primary dendrites of HCs. These bulbs are in an OPL stratum well below the cone axon terminal base and make contacts with other HCs and CBCs. Our results from immunolabeling, electron microscopy, and glutamate imaging suggest that HC bulbs represent GABAergic synapses that do not receive any direct photoreceptor input. Together, our data suggest the existence of two synaptic strata in the mouse OPL, spatially separating cone-specific feedback and feedforward signaling to CBCs. A biophysical model of a HC dendritic branch and voltage imaging support the hypothesis that this spatial arrangement of synaptic contacts allows for simultaneous local feedback and global feedforward signaling by HCs.

Identifiants

DOI: 10.1016/j.cub.2021.11.055 PMID: 34910950 PMC: PMC8886496
pubmed: 34910950
pii: S0960-9822(21)01641-9
doi: 10.1016/j.cub.2021.11.055
pmc: PMC8886496
mid: NIHMS1773900
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

545-558.e5

Subventions

Organisme : NIBIB NIH HHS
ID : R01 EB027145
Pays : United States
Organisme : NINDS NIH HHS
ID : U01 NS113294
Pays : United States
Organisme : NINDS NIH HHS
ID : U01 NS118288
Pays : United States
Organisme : NIMH NIH HHS
ID : U19 MH114830
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2021 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Christian Behrens (C)

Institute for Ophthalmic Research, University of Tübingen, Elfriede-Aulhorn-Str. 7, 72076 Tübingen, Germany; Center for Integrative Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Bernstein Center for Computational Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Graduate Training Centre of Neuroscience, University of Tübingen, Otfried-Müller-Str. 27, 72076 Tübingen, Germany.

Shubhash Chandra Yadav (SC)

Neurosensorics/Animal Navigation, Institute for Biology and Environmental Sciences, University of Oldenburg, Carl-von-Ossietzky-Str. 9-11, 26111 Oldenburg, Germany.

Maria M Korympidou (MM)

Institute for Ophthalmic Research, University of Tübingen, Elfriede-Aulhorn-Str. 7, 72076 Tübingen, Germany; Center for Integrative Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Graduate Training Centre of Neuroscience, University of Tübingen, Otfried-Müller-Str. 27, 72076 Tübingen, Germany.

Yue Zhang (Y)

Institute for Ophthalmic Research, University of Tübingen, Elfriede-Aulhorn-Str. 7, 72076 Tübingen, Germany; Center for Integrative Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Graduate Training Centre of Neuroscience, University of Tübingen, Otfried-Müller-Str. 27, 72076 Tübingen, Germany.

Silke Haverkamp (S)

Department of Computational Neuroethology, Center of Advanced European Studies and Research (caesar), Ludwig-Erhard-Allee 2, 53175 Bonn, Germany.

Stephan Irsen (S)

Electron Microscopy and Analytics, Center of Advanced European Studies and Research (caesar), Ludwig-Erhard-Allee 2, 53175 Bonn, Germany.

Anna Schaedler (A)

Institute for Ophthalmic Research, University of Tübingen, Elfriede-Aulhorn-Str. 7, 72076 Tübingen, Germany; Center for Integrative Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Graduate Training Centre of Neuroscience, University of Tübingen, Otfried-Müller-Str. 27, 72076 Tübingen, Germany.

Xiaoyu Lu (X)

Systems, Synthetic, and Physical Biology Program, Rice University, 6500 Main St., Houston, TX 77005, USA.

Zhuohe Liu (Z)

Department of Electrical and Computer Engineering, Rice University, 6100 Main St., Houston, TX 77005, USA.

Jan Lause (J)

Institute for Ophthalmic Research, University of Tübingen, Elfriede-Aulhorn-Str. 7, 72076 Tübingen, Germany; Center for Integrative Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Bernstein Center for Computational Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Graduate Training Centre of Neuroscience, University of Tübingen, Otfried-Müller-Str. 27, 72076 Tübingen, Germany.

François St-Pierre (F)

Systems, Synthetic, and Physical Biology Program, Rice University, 6500 Main St., Houston, TX 77005, USA; Department of Electrical and Computer Engineering, Rice University, 6100 Main St., Houston, TX 77005, USA; Department of Neuroscience, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA; Biochemistry and Molecular Biology, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.

Katrin Franke (K)

Institute for Ophthalmic Research, University of Tübingen, Elfriede-Aulhorn-Str. 7, 72076 Tübingen, Germany; Center for Integrative Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Bernstein Center for Computational Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany.

Anna Vlasits (A)

Institute for Ophthalmic Research, University of Tübingen, Elfriede-Aulhorn-Str. 7, 72076 Tübingen, Germany; Center for Integrative Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Bernstein Center for Computational Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany.

Karin Dedek (K)

Neurosensorics/Animal Navigation, Institute for Biology and Environmental Sciences, University of Oldenburg, Carl-von-Ossietzky-Str. 9-11, 26111 Oldenburg, Germany.

Robert G Smith (RG)

Department of Neuroscience, University of Pennsylvania, 422 Curie Blvd, Philadelphia, PA 19104, USA.

Thomas Euler (T)

Institute for Ophthalmic Research, University of Tübingen, Elfriede-Aulhorn-Str. 7, 72076 Tübingen, Germany; Center for Integrative Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Bernstein Center for Computational Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany.

Philipp Berens (P)

Institute for Ophthalmic Research, University of Tübingen, Elfriede-Aulhorn-Str. 7, 72076 Tübingen, Germany; Center for Integrative Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Bernstein Center for Computational Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany; Tübingen AI Center, University of Tübingen, Maria-von-Linden-Straße 6, 72076 Tübingen, Germany.

Timm Schubert (T)

Institute for Ophthalmic Research, University of Tübingen, Elfriede-Aulhorn-Str. 7, 72076 Tübingen, Germany; Center for Integrative Neuroscience, University of Tübingen, Otfried-Müller-Str. 25, 72076 Tübingen, Germany. Electronic address: timm.schubert@cin.uni-tuebingen.de.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Retinal horizontal cells use different...
questionsmedicales.fr › Sciences de l'information › Analyse des systèmes › Recherche opérationnelle › Rétroaction › Retinal horizontal cells use different...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Retinal horizontal cells use different...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Retinal horizontal cells use different...
questionsmedicales.fr › Organes des sens › Oeil › Rétine › Retinal horizontal cells use different...
questionsmedicales.fr › Cellules › Neurones › Neurones afférents › Cellules réceptrices sensorielles › Cellules photoréceptrices › Cellules photoréceptrices de vertébré › Cellules photoréceptrices en cône de la rétine › Retinal horizontal cells use different...
questionsmedicales.fr › Cellules › Neurones › Neurones afférents › Neurones rétiniens › Cellules horizontales de la rétine › Retinal horizontal cells use different...
questionsmedicales.fr › Cellules › Structures cellulaires › Membrane cellulaire › Structures de la membrane cellulaire › Jonctions intercellulaires › Synapses › Retinal horizontal cells use different...