Revealing sound-induced motion patterns in fish hearing structures in 4D: a standing wave tube-like setup designed for high-resolution time-resolved tomography

Abstract

Modern bony fishes possess a high morphological diversity in the auditory structures and their auditory capabilities. Yet, our knowledge of how the auditory structures such as the otoliths in the inner ears and the swim bladder work together remains elusive. Gathering experimental evidence on the in-situ motion of fish auditory structures while avoiding artifacts caused by surgical exposure of the structures has been challenging for decades. Synchrotron radiation-based tomography with high spatio-temporal resolution allows to study morphofunctional issues non-invasively in an unprecedented way. We therefore aimed to develop an approach that characterizes the moving structures in 4D (= three spatial dimensions+time). We designed a miniature standing wave tube-like setup to meet both the requirements of tomography and those of tank acoustics. With this new setup, we successfully visualized the motion of isolated otoliths and the auditory structures in zebrafish (Danio rerio) and the glass catfish (Kryptopterus vitreolus).

Hearing in catfishes: 200 years of research

“…The endolymphatic fluid flow from the transverse canal into the saccules resulted in a tilting and dorsoventral motion of the sagittae, which most likely stimulates sensory hair cells due to the vertically oriented ciliary bundles. Synchrotron radiation‐based tomography with high spatio‐temporal resolution showed in the glass catfish Kryptopterus vitreolus (Siluridae) a rotational movement of the sagittae, similar to goldfish (Maiditsch et al, 2022 ) (Figure 4 ). This supports the hypothesis that the otophysan saccule is an endorgan specialized to detect sound pressure, whereas the lagena and utricle detect particle motion.…”

“…Subsequently, it is possible to determine which sound component affects the motion of auditory structures. (Siluridae) a rotational movement of the sagittae, similar to goldfish (Maiditsch et al, 2022) (Figure 4). This supports the hypothesis that the otophysan saccule is an endorgan specialized to detect sound pressure, whereas the lagena and utricle detect particle motion.…”

“…The overlay of outer contours of otoliths reveals slight rotational movement of sagittae. Modified after Maiditsch et al ( 2022 ). See also film clip in supplements of this paper.…”

Functional plasticity of the swim bladder as an acoustic organ for communication in a vocal fish

“…To validate our model's findings, future experiments that investigate the response of the inner ear otolithic end organs to sound pressure stimuli, such as that produced and controlled in a standing wave tube-like system, coupled with relatively high speed (approx. 100 fps) X-ray phase contrast imaging to track otolith motion over time [ 68 , 69 ], should be conducted to determine how the inner ear end organs respond to both sound pressure and particle motion signals.…”

Swim bladder resonance enhances hearing in crucian carp (Carassius auratus)

“…Using traditional surgical methods to investigate the motion of the otoliths are challenging because of the limitation of inserting recorder into the specimen. Recently, a new experimental setup was used to visualize the motion of the isolated otoliths in 4D, providing insights into the motion of auditory structures (Maiditsch et al, 2022). Besides, finite element modeling offers an alternative way to study the roles of the otoliths in fish hearing and has been widely used in odontocetes to investigate sound transmission and reception (Cranford and Krysl, 2015; Song et al, 2021; Tubelli et al, 2018), which may facilitate more studies on hearing mechanism in fish.…”