Abstract
Hearing is a crucial sense in underwater environments for communication, hunting, attracting mates, and detecting predators. However, the tools currently used to study hearing are limited, as they cannot controllably stimulate specific parts of the auditory system. To date, the contributions of hearing organs have been identified through lesion experiments that inactivate an organ, making it difficult to gauge the specific stimuli to which each organ is sensitive, or the ways in which inputs from multiple organs are combined during perception. Here, we introduce Bio-Opto-Acoustic (BOA) stimulation, using optical forces to generate localized vibrations in vivo, and demonstrate stimulation of the auditory system of zebrafish larvae with precise control. We use a rapidly oscillated optical trap to generate vibrations in individual otolith organs that are perceived as sound, while adjacent otoliths are either left unstimulated or similarly stimulated with a second optical laser trap. The resulting brain-wide neural activity is characterized using fluorescent calcium indicators, thus linking each otolith organ to its individual neuronal network in a way that would be impossible using traditional sound delivery methods. The results reveal integration and cooperation of the utricular and saccular otoliths, which were previously described as having separate biological functions, during hearing.
Highlights
Hearing is a crucial sense in underwater environments for communication, hunting, attracting mates, and detecting predators
Otoliths, which are attached to sensory hair cells, move and vibrate in response to mechanical waves, which allow the detection of acceleration and variable sound frequencies
Because of the challenges of stimulating individual auditory organs in aquatic animals, the utricle’s and saccule’s specific contributions to hearing have remained uncertain. Since both the vestibular and auditory systems rely on these two pairs of otoliths at this stage of development[29], this uncertainty extends across two sensory modalities, with a consensus that the utricular otolith is used principally for vestibular perception and the saccular principally for audition[30,31,32]
Summary
Hearing is a crucial sense in underwater environments for communication, hunting, attracting mates, and detecting predators. Zebrafish larvae are a powerful model system for studying brain-wide neural networks in general, and sensory networks in particular[22] They offer a relatively simple auditory system with only two pairs of otoliths (utricular and saccular), and a lateral line for low frequencies[23]. Because of the challenges of stimulating individual auditory organs in aquatic animals, the utricle’s and saccule’s specific contributions to hearing have remained uncertain Since both the vestibular and auditory systems rely on these two pairs of otoliths at this stage of development[29], this uncertainty extends across two sensory modalities, with a consensus that the utricular otolith is used principally for vestibular perception and the saccular principally for audition[30,31,32]. This, in turn, allowed the targeted and systematic exploration of the contributions made by individual auditory organs to auditory and vestibular perception in this important model system
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