Optogenetic activation of serotonergic neurons changes masticatory movement in freely moving mice

Abstract The serotonergic system modulates the neural circuits involved in jaw movement; however, the role of serotonin (5-HT) neurons in masticatory movement remains unclear. Here, we investigated the effect of selective activation of 5-HT neurons in the dorsal raphe nucleus (DRN), or the raphe obs...

Full description

Saved in:
Bibliographic Details
Main Authors: Masanori Dantsuji, Ayako Mochizuki, Kiyomi Nakayama, Mitsuko Kanamaru, Masahiko Izumizaki, Kenji F. Tanaka, Tomio Inoue, Shiro Nakamura
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-024-79429-5
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850184679617986560
author Masanori Dantsuji
Ayako Mochizuki
Kiyomi Nakayama
Mitsuko Kanamaru
Masahiko Izumizaki
Kenji F. Tanaka
Tomio Inoue
Shiro Nakamura
author_facet Masanori Dantsuji
Ayako Mochizuki
Kiyomi Nakayama
Mitsuko Kanamaru
Masahiko Izumizaki
Kenji F. Tanaka
Tomio Inoue
Shiro Nakamura
author_sort Masanori Dantsuji
collection DOAJ
description Abstract The serotonergic system modulates the neural circuits involved in jaw movement; however, the role of serotonin (5-HT) neurons in masticatory movement remains unclear. Here, we investigated the effect of selective activation of 5-HT neurons in the dorsal raphe nucleus (DRN), or the raphe obscurus nucleus (ROb), on voluntary masticatory movement using transgenic mice expressing the channelrhodopsin-2 (ChR2) mutant (C128S) in central 5-HT neurons. During voluntary mastication, DRN blue light illumination increased masticatory frequency and decreased the root mean square peak amplitude of electromyography (EMG) in the masseter muscles. DRN blue light illumination also decreased EMG burst duration in the masseter and digastric muscles. These changes were blocked by a 5-HT2A receptor antagonist. Conversely, ROb blue light illumination during voluntary mastication did not affect masticatory frequency and EMG bursts in the masseter and digastric muscles. DRN or ROb blue light illumination during the resting state did not induce rhythmic jaw movement such as mastication but induced an increase in EMG activity in masseter and digastric muscles. These results suggest that both DRN and ROb 5-HT neurons may facilitate jaw movement. Furthermore, DRN 5-HT neuron may contribute to changes in masticatory patterns during the masticatory sequence.
format Article
id doaj-art-80e1bd2e36e94e95a63fb8a8b7005d58
institution OA Journals
issn 2045-2322
language English
publishDate 2024-11-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj-art-80e1bd2e36e94e95a63fb8a8b7005d582025-08-20T02:16:59ZengNature PortfolioScientific Reports2045-23222024-11-0114111410.1038/s41598-024-79429-5Optogenetic activation of serotonergic neurons changes masticatory movement in freely moving miceMasanori Dantsuji0Ayako Mochizuki1Kiyomi Nakayama2Mitsuko Kanamaru3Masahiko Izumizaki4Kenji F. Tanaka5Tomio Inoue6Shiro Nakamura7Department of Oral Physiology, Showa University School of DentistryDepartment of Oral Physiology, Showa University School of DentistryDepartment of Oral Physiology, Showa University School of DentistryFaculty of Arts and Sciences at Fujiyoshida, Showa UniversityDepartment of Physiology, Showa University School of MedicineDivision of Brain Sciences, Institute for Advanced Medical Research, Keio University School of MedicineDepartment of Oral Physiology, Showa University School of DentistryDepartment of Oral Physiology, Showa University School of DentistryAbstract The serotonergic system modulates the neural circuits involved in jaw movement; however, the role of serotonin (5-HT) neurons in masticatory movement remains unclear. Here, we investigated the effect of selective activation of 5-HT neurons in the dorsal raphe nucleus (DRN), or the raphe obscurus nucleus (ROb), on voluntary masticatory movement using transgenic mice expressing the channelrhodopsin-2 (ChR2) mutant (C128S) in central 5-HT neurons. During voluntary mastication, DRN blue light illumination increased masticatory frequency and decreased the root mean square peak amplitude of electromyography (EMG) in the masseter muscles. DRN blue light illumination also decreased EMG burst duration in the masseter and digastric muscles. These changes were blocked by a 5-HT2A receptor antagonist. Conversely, ROb blue light illumination during voluntary mastication did not affect masticatory frequency and EMG bursts in the masseter and digastric muscles. DRN or ROb blue light illumination during the resting state did not induce rhythmic jaw movement such as mastication but induced an increase in EMG activity in masseter and digastric muscles. These results suggest that both DRN and ROb 5-HT neurons may facilitate jaw movement. Furthermore, DRN 5-HT neuron may contribute to changes in masticatory patterns during the masticatory sequence.https://doi.org/10.1038/s41598-024-79429-5MasticationSerotoninDorsal rapheChannelrhodopsinsOptogeneticsElectromyography
spellingShingle Masanori Dantsuji
Ayako Mochizuki
Kiyomi Nakayama
Mitsuko Kanamaru
Masahiko Izumizaki
Kenji F. Tanaka
Tomio Inoue
Shiro Nakamura
Optogenetic activation of serotonergic neurons changes masticatory movement in freely moving mice
Scientific Reports
Mastication
Serotonin
Dorsal raphe
Channelrhodopsins
Optogenetics
Electromyography
title Optogenetic activation of serotonergic neurons changes masticatory movement in freely moving mice
title_full Optogenetic activation of serotonergic neurons changes masticatory movement in freely moving mice
title_fullStr Optogenetic activation of serotonergic neurons changes masticatory movement in freely moving mice
title_full_unstemmed Optogenetic activation of serotonergic neurons changes masticatory movement in freely moving mice
title_short Optogenetic activation of serotonergic neurons changes masticatory movement in freely moving mice
title_sort optogenetic activation of serotonergic neurons changes masticatory movement in freely moving mice
topic Mastication
Serotonin
Dorsal raphe
Channelrhodopsins
Optogenetics
Electromyography
url https://doi.org/10.1038/s41598-024-79429-5
work_keys_str_mv AT masanoridantsuji optogeneticactivationofserotonergicneuronschangesmasticatorymovementinfreelymovingmice
AT ayakomochizuki optogeneticactivationofserotonergicneuronschangesmasticatorymovementinfreelymovingmice
AT kiyominakayama optogeneticactivationofserotonergicneuronschangesmasticatorymovementinfreelymovingmice
AT mitsukokanamaru optogeneticactivationofserotonergicneuronschangesmasticatorymovementinfreelymovingmice
AT masahikoizumizaki optogeneticactivationofserotonergicneuronschangesmasticatorymovementinfreelymovingmice
AT kenjiftanaka optogeneticactivationofserotonergicneuronschangesmasticatorymovementinfreelymovingmice
AT tomioinoue optogeneticactivationofserotonergicneuronschangesmasticatorymovementinfreelymovingmice
AT shironakamura optogeneticactivationofserotonergicneuronschangesmasticatorymovementinfreelymovingmice