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

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 and Gilles Laurent ()
Additional contact information
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
Tatiana Gallego-Flores: Max Planck Institute for Brain Research
David Hain: Max Planck Institute for Brain Research
Sam Reiter: Max Planck Institute for Brain Research
Riho Kobayashi: Max Planck Institute for Brain Research
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

Nature, 2020, vol. 578, issue 7795, 413-418

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41586-020-1993-6

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