Organization of subcortical auditory nuclei of Japanese house bat (Pipistrellus abramus) identified with cytoarchitecture and molecular expression

Abstract

The auditory system of echolocating bats shows remarkable specialization likely related to analyzing echoes of sonar pulses. However, significant interspecies differences have been observed in the organization of auditory pathways among echolocating bats, and the homology of auditory nuclei with those of non-echolocating species has not been established. Here, in order to establish the homology and specialization of auditory pathways in echolocating bats, the expression of markers for glutamatergic, GABAergic, and glycinergic phenotypes in the subcortical auditory nuclei of Japanese house bat (Pipistrellus abramus) was evaluated. In the superior olivary complex, we identified the medial superior olive and superior paraolivary nuclei as expressing glutamatergic and GABAergic phenotypes, respectively, suggesting these nuclei are homologous with those of rodents. In the nuclei of the lateral lemniscus (NLL), the dorsal nucleus was found to be purely GABAergic, the intermediate nucleus was a mixture of glutamatergic and inhibitory neurons, the compact part of the ventral nucleus was purely glycinergic, and the multipolar part of the ventral nucleus expressed both GABA and glycine. In the inferior colliculus (IC), the central nucleus was found to be further subdivided into dorsal and ventral parts according to differences in the density of terminals and the morphology of large GABAergic neurons, suggesting specialization to sonar pulse structure. Medial geniculate virtually lacked GABAergic neurons, suggesting that the organization of the tectothalamic pathway is similar with that of rodents. Taken together, our findings revealed that specialization primarily occurs with regard to nuclei size and organization of the NLL and IC.

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

“…The distinction between the MSO and DPO can be very difficult in bats, as these nuclei are sometimes closely attached to each other. Here, we identify the MSO and show, as described in other bats (Gibbons et al., 2020; Grothe et al., 1994; Ito, Furuyama, Hase, Kobayasi, Hiryu, et al., 2018; Zook & Casseday, 1982a), that its neurons are not orderly aligned in one plane like in low‐frequency hearing mammals (Henkel & Brunso‐Bechtold, 1990; Kulesza, 2007; Rautenberg et al., 2009; Stotler, 1953) and even the MSO itself appears in some sections split into a lateral and medial part. Nevertheless, the intensity differences of the VGlut1 labeling in conjuncture with GlyT2 labeling differentiates the MSO from the DPO.…”

“…Separating the INLL from the dorsal VNLL is difficult in most mammals, as the boundary is not well defined and both nuclei appear to merge. In rodents and in bats, this merging is, however, misleading, because VNLL neurons are GABAergic and glycinergic, while a large fraction of INLL neurons express glutamatergic markers (Ito et al., 2011; Ito, Furuyama, Hase, Kobayasi, Hiryu, et al., 2018), a finding consistent with the absence of inhibitory markers in cat (Saint Marie et al., 1997). A sometimes‐used landmark for segregation is a characteristic curvature of the outer shape of the brain sections.…”

“…Due to their exquisite auditory system and the ability to perform echolocation, bats serve as a model system for auditory research. In various bat species, the auditory brainstem has been characterized by fiber tracing (e.g., Grothe et al., 1994; Schweizer, 1981; Vater & Feng, 1990; Zook & Casseday, 1982b), immunohistochemistry (e.g., Ito, Furuyama, Hase, Kobayasi, Hiryu, et al., 2018; Rosenberger et al., 2003; Vater & Braun, 1994), and electrophysiology (e.g., Covey & Casseday, 1991; Grothe, 1994; Portfors & Wenstrup, 2001; Yang & Pollak, 1994b). These characterizations have highlighted the structure–function relation of neurons in the SOC and lateral lemniscus (LL).…”

Auditory communication processing in bats: What we know and where to go.

“…The IC is a midbrain structure that serves as a hub for auditory information processing. It receives ascending input from brain stem nuclei (Casseday, Fremouw, & Covey, 2002; Ito, Furuyama, Hase, Kobayasi, & Hiryu, 2018; Ito, Furuyama, Hase, Kobayasi, Hiryu, & Riquimaroux, 2018; Pollak, Wenstrup, & Fuzessey, 1986) as well as descending input from the auditory cortex (E. Gao & Suga, 1998; X.…”

Inhibitory Neural Circuits in the Mammalian Auditory Midbrain

“…The 3 cell types in the IC (LG, SG, and glutamatergic cells) are found in many amniote species, including the chicken, pigeon, bat, rat, mouse, common marmoset, and Japanese macaque. 81,44,45,123,124 This strongly suggests that the organization of cell types in the IC evolved at least 300 million years ago when the common ancestor of reptiles and mammals (stem amniotes) emerged. At this point, there is no information about the presence of the 3 cell types in the anamniote IC.…”