Experience shapes chandelier cell function and structure in the visual cortex

Koen Seignette, Nora Jamann, Paolo Papale, Huub Terra, Ralph O. Porneso, Leander de Kraker, Chris van der Togt, Maaike van der Aa, Paul Neering, Emma Ruimschotel, Pieter R. Roelfsema, Jorrit S. Montijn, Matthew W. Self, Maarten H.P. Kole, Christiaan N. Levelt

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Detailed characterization of interneuron types in primary visual cortex (V1) has greatly contributed to understanding visual perception, yet the role of chandelier cells (ChCs) in visual processing remains poorly characterized. Using viral tracing we found that V1 ChCs predominantly receive monosynaptic input from local layer 5 pyramidal cells and higher-order cortical regions. Two-photon calcium imaging and convolutional neural network modeling revealed that ChCs are visually responsive but weakly selective for stimulus content. In mice running in a virtual tunnel, ChCs respond strongly to events known to elicit arousal, including locomotion and visuomotor mismatch. Repeated exposure of the mice to the virtual tunnel was accompanied by reduced visual responses of ChCs and structural plasticity of ChC boutons and axon initial segment length. Finally, ChCs only weakly inhibited pyramidal cells. These findings suggest that ChCs provide an arousal-related signal to layer 2/3 pyramidal cells that may modulate their activity and/or gate plasticity of their axon initial segments during behaviorally relevant events.

Original languageEnglish
Article numberRP91153
Pages (from-to)1-34
Number of pages34
JournaleLife
Volume12
DOIs
Publication statusPublished - 9 Jan 2024

Bibliographical note

Publisher Copyright:
© 2023, Seignette et al.

Funding

We thank all members of the Levelt lab for discussion and support. We thank staff of the animal facility and mechatronics department at the Netherlands Institute for Neuroscience for technical support. We thank Dr. Seungho Lee from Pohang University of Science and Technology for kindly providing viral vectors for rabies tracing experiments and Dr. Hongkui Zeng and the Allen Institute for Brain Science for providing the Vipr2-Cre mice. We thank Dr. Maren Engelhardt for providing the Rabbit-β-IV-Spectrin antibody, Barbara Hobo for help with tail vein injections, Ulrike Schlegel for help with QUINT software, and David van Oorschot and Dilara Ilhan for help with experiments. We are grateful to Dr. Jean-Charles Paterna and Dr. Melanie Rauch from the Viral Vector Facility VVF at the ETH Zurich and University of Zurich for their expert advice, support, and services regarding viral vector production. This project received funding from the European Union’s Horizon 2020 Research and Innovation Program under grant agreement nos. 785907 (HBP SGA2, CL & PR) and 945539 (HBP SGA3, CL & PR), from the Dutch Research Council (NWO-OCENW.KLEIN.178, CL & PR and FlagEra SoundSight, 680-91-320, CL). The authors declare that they have no competing interests. All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials.

FundersFunder number
Allen Institute for Brain Science
FlagEra SoundSight680-91-320
NWO-OCENW
Horizon 2020 Framework Programme785907, 945539
Pohang University of Science and Technology
Eidgenössische Technische Hochschule Zürich
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Universität Zürich

    Keywords

    • arousal
    • axo-axonic
    • chandelier
    • inhibitition
    • most exciting input
    • mouse
    • neuroscience
    • prediction error

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