The continued importance of comparative auditory research to modern scientific discovery

Abstract

A rich history of comparative research in the auditory field has afforded a synthetic view of sound information processing by ears and brains. Some organisms have proven to be powerful models for human hearing due to fundamental similarities (e.g., well-matched hearing ranges), while others feature intriguing differences (e.g., atympanic ears) that invite further study. Work across diverse "non-traditional" organisms, from small mammals to avians to amphibians and beyond, continues to propel auditory science forward, netting a variety of biomedical and technological advances along the way. In this brief review, limited primarily to tetrapod vertebrates, we discuss the continued importance of comparative studies in hearing research from the periphery to central nervous system with a focus on outstanding questions such as mechanisms for sound capture, peripheral and central processing of directional/spatial information, and non-canonical auditory processing, including efferent and hormonal effects.

Keywords: Auditory system; Bone conduction; Comparative biology; Directional hearing; Ears; Hearing.

Figure 1:. Tympanic middle ears vary among tetrapods and are hypothesized to have arisen evolutionarily at least three times.

A simplified cladogram representing the evolutionary relationships among the four main tetrapod groups (Amphibia, Lepidosauria, Archosauria, and Mammalia). Species diversity and the estimated percent of acoustically communicating species are displayed above each group (data derived from Chen and Wiens (2020)). Black ovals indicate the independent evolutionary origins of tympanic middle ears. Top diagrams show a glimpse of middle ear diversity seen across tetrapods. Abbreviations: AB: auditory bulla, EAC: external auditory canal, ES: extrastapes, ET: Eustachian tube, IE: inner ear, In: incus, LJ: lower jaw, Ma: malleus, MEC: middle ear cavity, Op: operculum, Qu: quadrate, St: stapes, TM: tympanum,

Figure 2:. Directional hearing.

A, Averaged ITD tuning curves in midbrain tegmentum reveal neural responses like the opponent-channel code hypothesized in mammals in left (red) and right (blue) hemispheres. The curves cross at the midline and the steepest slopes are positioned within the physiological range (black dashed lines). Modified from Peña et al., 2019 and Cazettes et al., 2018. B, Directional responses of auditory nerve fibers in the gecko. Combination line and histogram plot of the distribution of spatial receptive field sizes for all fibers. Recordings shown from the right auditory nerve (red, data were reflected to simulate left side responses in blue). From Christensen-Dalsgaard et al., 2021.

Figure 3:. Generalized brainstem organization of the vertebrate octavolateral efferent system.

Auditory (filled circles) and vestibular (open circles) efferent neurons send projections (red) to peripheral sensory hair cells to modulate afferent inputs (blue). Abbrev: HC: hair cell (IHC: inner hair cell, OHC: outer hair cell, SHC: short hair cell, THC: tall hair cell), mlf: medial longitudinal fascicle, OC: olivocochlear (LOC: lateral olivocochlear, MOC: medial olivocochlear), V: trigeminal nucleus, VI abducens motor nucleus, VII: facial branchial motor nucleus.