PIEZO2 mediates ultrasonic hearing via cochlear outer hair cells in mice

Author:

Li Jie,Liu Shuang,Song Chenmeng,Hu Qun,Zhao Zhikai,Deng Tuantuan,Wang Yi,Zhu Tong,Zou Linzhi,Wang Shufeng,Chen Jiaofeng,Liu Lian,Hou Hanqing,Yuan Kexin,Zheng Hairong,Liu ZhiyongORCID,Chen Xiaowei,Sun Wenzhi,Xiao Bailong,Xiong Wei

Abstract

AbstractUltrasonic hearing is exploited for hunting and navigation as in echolocation by microbats and bottleneck dolphins, and for social communication like ultrasonic vocalization by mice and rats. However, the molecular and cellular basis for ultrasonic hearing is not known yet. Here we show that knockout of the mechanosensitive ion channel PIEZO2 in cochlea disrupts the ultrasonic hearing but not the low-frequency hearing in mice, as shown by audiometry and acoustically-associative freezing behavior. Deletion of Piezo2 in the outer hair cells specifically abolishes the associative learning of the mice upon hearing the ultrasonic frequency. Ex vivo cochlear Ca2+ imaging revealed that the ultrasonic transduction requires both PIEZO2 and the hair-cell mechanotransduction channel. Together, our study demonstrates that the outer hair cells are the effector cells with PIEZO2 as an essential molecule for ultrasonic hearing in mice.Significance StatementSome animals have evolved an incredible ability for vocalizing and hearing ultrasonic frequencies that is inaudible for humans (> 20 kHz). For many years, it has been considered that animals hear ultrasonic frequencies with their cochlear hair cells, using the identical set of mechanotransduction molecules in the hair bundles for hearing audible frequencies. Here, we show that the mice lacking the mechanosensitive ion channel PIEZO2 hardly hear ultrasonic frequencies, while can still be sensitive to audible frequencies. Thus, animals may use a partially different mechanism for sensing physiological ultrasound.

Publisher

Cold Spring Harbor Laboratory

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