Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Abstract

The earliest vertebrate ears likely subserved a gravistatic function for orientation in the aquatic environment. However, in addition to detecting acceleration created by the animal's own movements, the otolithic end organs that detect linear acceleration would have responded to particle movement created by external sources. The potential to identify and localize these external sources may have been a major selection force in the evolution of the early vertebrate ear and in the processing of sound in the central nervous system. The intrinsic physiological polarization of sensory hair cells on the otolith organs confers sensitivity to the direction of stimulation, including the direction of particle motion at auditory frequencies. In extant fishes, afferents from otolithic end organs encode the axis of particle motion, which is conveyed to the dorsal regions of first-order octaval nuclei. This directional information is further enhanced by bilateral computations in the medulla and the auditory midbrain. We propose that similar direction-sensitive neurons were present in the early aquatic tetrapods and that selection for sound localization in air acted upon preexisting brain stem circuits like those in fishes. With movement onto land, the early tetrapods may have retained some sensitivity to particle motion, transduced by bone conduction, and later acquired new auditory papillae and tympanic hearing. Tympanic hearing arose in parallel within each of the major tetrapod lineages and would have led to increased sensitivity to a broader frequency range and to modification of the preexisting circuitry for sound source localization.

Conserved and divergent development of brainstem vestibuloacoustic nuclei

“…NM cells originate from the caudal hindbrain, posterior to rhombomere 5 (Figures 4 F-K and 8 and (Cambronero and Puelles, 2000;Cramer et al, 2000;Marin and Puelles, 1995)), while SBCs originate from rostral rhombomeres (Di Bonito and Studer, 2017;Farago et al, 2006). This is in agreement with the proposition that NM cells derive from ancestral vestibuloacoustic cells of the caudal octaval column (previous section and (Carr and Christensen-Dalsgaard, 2016;Walton et al, 2017)), while SBCs may be an elaboration of components of an interaural level difference (ILD) circuit, which, in mammals, is proposed to predate the ITD circuit (Grothe and Pecka, 2014). The comparison of the developmental origin of NM neurons and SBCs thus supports an independent evolutionary origin for these functionally analogous cell types.…”

“…In zebrafish, Atoh1 is required for the development of a subpopulation of zn-5 + and Lhx2/9 + cells that may correspond to contralaterally projecting octaval neurons (Sassa et al, 2007) and preliminary mapping data shows Atoh1 labelling of neurons on the caudal octaval nucleus (Wullimann et al, 2011). Moreover, it has been proposed that NM neurons may derive from an ancestral population equivalent to extant neurons of the dorsal descending octaval nucleus of fish (Carr and Christensen-Dalsgaard, 2016;Walton et al, 2017), which are part of a binaural circuit that sharpens directional information from the saccule (Edds- Walton, 2016). Overall, this suggests that extant caudal octaval (vestibuloacoustic) neurons in chick that belong to the auditory NM and the vestibular DeV may be ancestrally related.…”

“…(Figure 1 D,E and (Carr and Soares, 2002)). However, the NL and MSO differ in their location within the brainstem (Figure 1 C,D and (Grothe et al, 2004)), employ differing neural coding strategies (Grothe and Pecka, 2014;Grothe et al, 2010) and most likely have separate evolutionary origins (Carr and Christensen-Dalsgaard, 2016;Grothe et al, 2004;Grothe and Pecka, 2014;Walton et al, 2017). In mammals, the MSO is proposed to be an elaboration of the LSO which computes ILDs (Grothe and Pecka, 2014).…”

Neural Maps of Interaural Time Difference in the American Alligator: A Stable Feature in Modern Archosaurs

“…In mammals, ITDs are not arranged in a topographically organized map at either the level of ITD processing in the auditory brainstem (Karino et al, 2011;Grothe and Pecka, 2014) or at higher processing stages, including the superior colliculus (Campbell et al, 2006). These differences are the likely consequence of the parallel evolutionary origins of spatial hearing in mammals and birds (for reviews, see Christensen-Dalsgaard and Carr, 2008;Grothe and Pecka, 2014;Walton et al, 2017;Lingner et al, 2018). Overall, archosaurs, including birds, and mammals can both localize sounds in space, but use different neuronal strategies to encode sound location.…”

“…Loss of coupling would have changed the role of the central auditory system from enhancing a preexisting directional signal to computing a directional signal. Coding of sound source location therefore differs between archosaurs and lizards, with lizards having a directional input from the auditory nerve (Christensen-Dalsgaard et al, 2011) and a relatively small first-order nucleus magnocellularis and NL (Tang et al, 2012), whereas birds (and now alligators) have a less directional signal from the periphery and a larger nucleus magnocellularis and NL (Walton et al, 2017).…”