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A claustrum in reptiles and its role in slow-wave sleep

Author

Listed:
  • Hiroaki Norimoto

    (Max Planck Institute for Brain Research)

  • Lorenz A. Fenk

    (Max Planck Institute for Brain Research)

  • Hsing-Hsi Li

    (Max Planck Institute for Brain Research)

  • Maria Antonietta Tosches

    (Max Planck Institute for Brain Research
    Columbia University)

  • Tatiana Gallego-Flores

    (Max Planck Institute for Brain Research)

  • David Hain

    (Max Planck Institute for Brain Research
    Goethe University)

  • Sam Reiter

    (Max Planck Institute for Brain Research
    Okinawa Institute of Science and Technology Graduate University)

  • Riho Kobayashi

    (Max Planck Institute for Brain Research
    Nagoya City University)

  • Angeles Macias

    (Max Planck Institute for Brain Research)

  • Anja Arends

    (Max Planck Institute for Brain Research)

  • Michaela Klinkmann

    (Max Planck Institute for Brain Research)

  • Gilles Laurent

    (Max Planck Institute for Brain Research)

Abstract

The mammalian claustrum, owing to its widespread connectivity with other forebrain structures, has been hypothesized to mediate functions that range from decision-making to consciousness1. Here we report that a homologue of the claustrum, identified by single-cell transcriptomics and viral tracing of connectivity, also exists in a reptile—the Australian bearded dragon Pogona vitticeps. In Pogona, the claustrum underlies the generation of sharp waves during slow-wave sleep. The sharp waves, together with superimposed high-frequency ripples2, propagate to the entire neighbouring pallial dorsal ventricular ridge (DVR). Unilateral or bilateral lesions of the claustrum suppress the production of sharp-wave ripples during slow-wave sleep in a unilateral or bilateral manner, respectively, but do not affect the regular and rapidly alternating sleep rhythm that is characteristic of sleep in this species3. The claustrum is thus not involved in the generation of the sleep rhythm itself. Tract tracing revealed that the reptilian claustrum projects widely to a variety of forebrain areas, including the cortex, and that it receives converging inputs from, among others, areas of the mid- and hindbrain that are known to be involved in wake–sleep control in mammals4–6. Periodically modulating the concentration of serotonin in the claustrum, for example, caused a matching modulation of sharp-wave production there and in the neighbouring DVR. Using transcriptomic approaches, we also identified a claustrum in the turtle Trachemys scripta, a distant reptilian relative of lizards. The claustrum is therefore an ancient structure that was probably already present in the brain of the common vertebrate ancestor of reptiles and mammals. It may have an important role in the control of brain states owing to the ascending input it receives from the mid- and hindbrain, its widespread projections to the forebrain and its role in sharp-wave generation during slow-wave sleep.

Suggested Citation

  • Hiroaki Norimoto & Lorenz A. Fenk & Hsing-Hsi Li & Maria Antonietta Tosches & Tatiana Gallego-Flores & David Hain & Sam Reiter & Riho Kobayashi & Angeles Macias & Anja Arends & Michaela Klinkmann & Gi, 2020. "A claustrum in reptiles and its role in slow-wave sleep," Nature, Nature, vol. 578(7795), pages 413-418, February.
  • Handle: RePEc:nat:nature:v:578:y:2020:i:7795:d:10.1038_s41586-020-1993-6
    DOI: 10.1038/s41586-020-1993-6
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    Cited by:

    1. Guihua Xiao & Yeyi Cai & Yuanlong Zhang & Jingyu Xie & Lifan Wu & Hao Xie & Jiamin Wu & Qionghai Dai, 2024. "Mesoscale neuronal granular trial variability in vivo illustrated by nonlinear recurrent network in silico," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Gal Atlan & Noa Matosevich & Noa Peretz-Rivlin & Idit Marsh-Yvgi & Noam Zelinger & Eden Chen & Timna Kleinman & Noa Bleistein & Efrat Sheinbach & Maya Groysman & Yuval Nir & Ami Citri, 2024. "Claustrum neurons projecting to the anterior cingulate restrict engagement during sleep and behavior," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Layton Lamsam & Brett Gu & Mingli Liang & George Sun & Kamren J. Khan & Kevin N. Sheth & Lawrence J. Hirsch & Christopher Pittenger & Alfred P. Kaye & John H. Krystal & Eyiyemisi C. Damisah, 2024. "The human claustrum tracks slow waves during sleep," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    4. David Morizet & Isabelle Foucher & Alessandro Alunni & Laure Bally-Cuif, 2024. "Reconstruction of macroglia and adult neurogenesis evolution through cross-species single-cell transcriptomic analyses," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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