Structural arrangement of auditory brainstem nuclei in the bats Phyllostomus discolor and Carollia perspicillata

Abstract

The structure of the mammalian auditory brainstem is evolutionarily highly plastic, and distinct nuclei arrange in a species-dependent manner. Such anatomical variability is present in the superior olivary complex (SOC) and the nuclei of the lateral lemniscus (LL). Due to the structure-function relationship in the auditory brainstem, the identification of individual nuclei supports the understanding of sound processing. Here, we comparatively describe the nucleus arrangement and the expression of functional markers in the auditory brainstem of the two bat species Phyllostomus discolor and Carollia perspicillata. Using immunofluorescent labeling, we describe the arrangement and identity of the SOC and LL nuclei based on the expression of synaptic markers (vesicular glutamate transporter 1 and glycine transporter 2), calcium-binding proteins, as well as the voltage-gated ion channel subunits Kv1.1 and HCN1. The distribution of excitatory and inhibitory synaptic labeling appears similar between both species and matches with that of other mammals. The detection of calcium-binding proteins indicates species-dependent differences and deviations from other mammals. Kv1.1 and HCN1 show largely the same expression pattern in both species, which diverges from other mammals, indicating functional adaptations in the cellular physiology of bat neurons.

Molecular identity of the lateral lemniscus nuclei in the adult mouse brain

“…Calbindin immunoreactivity in neurons appears in the DLL and in a few VLL neurons of adult rats (Friauf, 1994), a pattern distinct to that observed in the mouse where Calb1 is expressed in the VLL and a few ILL neurons (present work). This latter pattern is on the whole similar to that described in two distant species, the mustached bat (Zettel et al, 1991) and the chinchilla (Kelley et al, 1992), although interspecies differences between bats have been reported (Pätz et al, 2022). These results suggest significant evolutionary differences in the expression of this molecule as previously proposed (Joven et al, 2013), in addition to the variations in Calbindin expression in the brain at different developmental stages including the auditory nuclei (Förster and Illing, 2000).…”

“…However, the ISH experiments analyzed in the present work seem to lack sensitivity to discern this gradient, which was witnessed through fluorescent immunohistochemistry. Alternatively, Hcn1 and the Kcna1 channel are expressed across the entire LLN in bats, a pattern that may be functionally related to the echolocation characteristic of these species ( Pätz et al, 2022 ).…”

“…This may be due to the VLL nuclei extending over several rhombomeres (r2-r4), such that the r2 and r3 parts of the VLL are evident in lateral planes whereas the r4 component of this nucleus is mainly seen in medial planes. The regions of expression in the VLL in which these genes might or might not be expressed could correspond to further subdivisions of the rodent VLL ( Caspari et al, 2015 ), as occurs in bats ( Ito et al, 2018 ; Pätz et al, 2022 ). We named these two subdivisions the rostral and caudal VLL, respectively, following the topological rostrocaudal axis of the brainstem that takes into account the pontine flexure ( Puelles et al, 2013 ).…”

Molecular and functional profiling of cell diversity and identity in the lateral superior olive, an auditory brainstem center with ascending and descending projections

“…Kcna1 |Kv1.1 was DEG#92 in pLSOs ( Figure 9A ). Kv α subunits have received extensive attention in the auditory brainstem, and immunoreactivity has been demonstrated in several species in somata, dendrites, and axon terminals (mouse: Wang et al, 1994 ; Brew et al, 2003 ; rat: Barnes-Davies et al, 2004 ; gerbil: Nabel et al, 2019 ); three bat species: ( Rosenberger et al, 2003 ; Pätz et al, 2022 ). Kv1.1 channels were most intensively analyzed.…”

Developmental profile of microglia distribution in nuclei of the superior olivary complex

“…No band was seen in VGluT1 knockout mice (manufacturer's datasheet). VGluT1 labels excitatory synaptic inputs in all major SOC nuclei of mice (Fischl et al., 2016), bats (Pätz et al., 2022), and in the MSO of gerbil (Callan et al., 2021).…”