Inaudible Airborne Ultrasound Affects Emotional States in the Olfactory Bulbectomized Rat Depression Model

Overview

Journal Sci Rep

Date 2025 Jan 25

PMID 39863793

Authors

Tsugumi Yamauchi

Kou Takahashi

Toshinori Yoshioka

Daisuke Yamada

Yoshio Nakano

Satoka Kasai

Satoshi Iriyama

Kazumi Yoshizawa

Shoichi Nishino

Satoru Miyazaki

Akiyoshi Saitoh

Affiliations

Soon will be listed here.

Abstract

Recently, exposure to sounds with ultrasound (US) components has been shown to modulate brain activity. However, the effects of US on emotional states remain poorly understood. We previously demonstrated that the olfactory bulbectomized (OBX) rat depression model is suitable for examining the effects of audible sounds on emotionality. Here, we investigated the impact of US exposure on the emotional state of OBX rats. In naive rats, exposure to 100 kHz US for 1 h did not increase the number of c-Fos-positive cells in auditory-related cortical areas, and US, as a tone cue, did not elicit a conditioned fear response in the auditory fear conditioning test. These results indicate that the frequency of 100 kHz is hard to hear for rats. However, US improved hyperemotionality (HE) scores and decreased plasma corticosterone levels in OBX rats, suggesting ameliorative effects on depression-like symptoms and stress. In contrast to HE scores, US exposure did not influence anxiety-like behaviors in the elevated plus maze. In conclusion, we demonstrated that exposure to airborne US can alleviate depressive-like symptoms in the OBX rat depression model. This is the first study to show that exposure to airborne US alone produces changes in emotional states in an animal model.

References

Lin L, Herselman M, Zhou X, Bobrovskaya L . Effects of corticosterone on BDNF expression and mood behaviours in mice. Physiol Behav. 2022; 247:113721. DOI: 10.1016/j.physbeh.2022.113721. View

Oohashi T, Nishina E, Honda M, Yonekura Y, Fuwamoto Y, Kawai N . Inaudible high-frequency sounds affect brain activity: hypersonic effect. J Neurophysiol. 2000; 83(6):3548-58. DOI: 10.1152/jn.2000.83.6.3548. View

Qiu Z, Guo J, Kala S, Zhu J, Xian Q, Qiu W . The Mechanosensitive Ion Channel Piezo1 Significantly Mediates In Vitro Ultrasonic Stimulation of Neurons. iScience. 2019; 21:448-457. PMC: 6849147. DOI: 10.1016/j.isci.2019.10.037. View

Du Y, Ping J, Li N, Wu X, Li L, Galbraith G . Ultrasonic evoked responses in rat cochlear nucleus. Brain Res. 2007; 1172:40-7. PMC: 2773379. DOI: 10.1016/j.brainres.2007.07.049. View

Kawai N, Honda M, Nishina E, Ueno O, Fukushima A, Ohmura R . Positive effect of inaudible high-frequency components of sounds on glucose tolerance: a quasi-experimental crossover study. Sci Rep. 2022; 12(1):18463. PMC: 9630438. DOI: 10.1038/s41598-022-23336-0. View

Kenet T, Froemke R, Schreiner C, Pessah I, Merzenich M . Perinatal exposure to a noncoplanar polychlorinated biphenyl alters tonotopy, receptive fields, and plasticity in rat primary auditory cortex. Proc Natl Acad Sci U S A. 2007; 104(18):7646-51. PMC: 1855918. DOI: 10.1073/pnas.0701944104. View

Wohr M, Schwarting R . Ultrasonic communication in rats: can playback of 50-kHz calls induce approach behavior?. PLoS One. 2007; 2(12):e1365. PMC: 2137933. DOI: 10.1371/journal.pone.0001365. View

Brenes J, Lackinger M, Hoglinger G, Schratt G, Schwarting R, Wohr M . Differential effects of social and physical environmental enrichment on brain plasticity, cognition, and ultrasonic communication in rats. J Comp Neurol. 2015; 524(8):1586-607. DOI: 10.1002/cne.23842. View

Kuribayashi R, Nittono H . High-Resolution Audio with Inaudible High-Frequency Components Induces a Relaxed Attentional State without Conscious Awareness. Front Psychol. 2017; 8:93. PMC: 5285336. DOI: 10.3389/fpsyg.2017.00093. View

10.

Brivio E, Lopez J, Chen A . Sex differences: Transcriptional signatures of stress exposure in male and female brains. Genes Brain Behav. 2020; 19(3):e12643. DOI: 10.1111/gbb.12643. View

11.

Ito M, Miyamae M, Yokoyama C, Yamashita Y, Ueno O, Maruo K . Augmentation of Positive Valence System-Focused Cognitive Behavioral Therapy by Inaudible High-Frequency Sounds for Anhedonia: A Trial Protocol for a Pilot Study. JAMA Netw Open. 2019; 2(11):e1915819. PMC: 6902816. DOI: 10.1001/jamanetworkopen.2019.15819. View

12.

Haragopal H, Mellott J, Dhar M, Kanel A, Mafi A, Tokar N . Tonotopic distribution and inferior colliculus projection pattern of inhibitory and excitatory cell types in the lateral superior olive of mice. J Comp Neurol. 2023; 531(14):1381-1388. PMC: 11571233. DOI: 10.1002/cne.25515. View

13.

Ghaderi A, Rosendahl I, Bohman B . Integrating motivational interviewing with cognitive behavioural therapy for anxiety disorders, depression and co-morbid unhealthy lifestyle behaviours: a randomised controlled pilot trial. Behav Cogn Psychother. 2021; 50(1):74-88. DOI: 10.1017/S1352465821000345. View

14.

Kuribayashi R, Yamamoto R, Nittono H . High-resolution music with inaudible high-frequency components produces a lagged effect on human electroencephalographic activities. Neuroreport. 2014; 25(9):651-5. DOI: 10.1097/WNR.0000000000000151. View

15.

Tsai C, Tsai S, Pan Y, Lin H, Pan T, Yang F . Transcranial Ultrasound Stimulation Reverses Behavior Changes and the Expression of Calcium-Binding Protein in a Rodent Model of Schizophrenia. Neurotherapeutics. 2022; 19(2):649-659. PMC: 9226253. DOI: 10.1007/s13311-022-01195-x. View

16.

Cahill B, Poelker-Wells S, Prather J, Li Y . A Glimpse Into the Sexual Dimorphisms in Major Depressive Disorder Through Epigenetic Studies. Front Neural Circuits. 2021; 15:768571. PMC: 8564393. DOI: 10.3389/fncir.2021.768571. View

17.

Thase M, Rush A . When at first you don't succeed: sequential strategies for antidepressant nonresponders. J Clin Psychiatry. 1997; 58 Suppl 13:23-9. View

18.

Oohashi T, Kawai N, Nishina E, Honda M, Yagi R, Nakamura S . The role of biological system other than auditory air-conduction in the emergence of the hypersonic effect. Brain Res. 2006; 1073-1074:339-47. DOI: 10.1016/j.brainres.2005.12.096. View

19.

Cain D, Cidlowski J . Immune regulation by glucocorticoids. Nat Rev Immunol. 2017; 17(4):233-247. PMC: 9761406. DOI: 10.1038/nri.2017.1. View

20.

Takahashi K, Murasawa H, Yamaguchi K, Yamada M, Nakatani A, Yoshida M . Riluzole rapidly attenuates hyperemotional responses in olfactory bulbectomized rats, an animal model of depression. Behav Brain Res. 2010; 216(1):46-52. DOI: 10.1016/j.bbr.2010.07.002. View