Organization of projection from brainstem auditory nuclei to the inferior colliculus of Japanese house bat (Pipistrellus abramus)

Abstract

ObjectivesEcholocating bats show remarkable specialization which is related to analysis of echoes of biosonars in subcortical auditory brainstem pathways. The inferior colliculus (IC) receives inputs from all lower brainstem auditory nuclei, i.e., cochlear nuclei, nuclei of the lateral lemniscus, and superior olivary complex, and create de novo responses to sound, which is considered crucial for echolocation. Inside the central nucleus of the IC (ICC), small domains which receive specific combination of extrinsic inputs are the basis of integration of sound information. In addition to extrinsic inputs, each domain is interconnected by local IC neurons but the cell types related to the interconnection are not well‐understood. The primary objective of the current study is to examine whether the ascending inputs are reorganized and terminate in microdomains inside the ICC.MethodsWe made injection of a retrograde tracer into different parts of the ICC, and analyzed distribution of retrogradely labeled cells in the auditory brainstem of Japanese house bat (Pipistrellus abramus).ResultsPattern of ascending projections from brainstem nuclei was similar to other bat species. Percentages of labeled cells in several nuclei were correlated each other. Furthermore, within the IC, we identified that large GABAergic (LG) and glutamatergic neurons made long‐range connection.ConclusionsSynaptic organization of IC of Japanese house bat shows specialization which is likely to relate for echolocation. Input nuclei to the IC make clusters which terminate in specific part of the ICC, implying the presence of microdomains. LG neurons have roles for binding IC microdomains.

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

“…VGLUT2+ axosomatic excitatory terminals on LG cells arise from various brainstem nuclei; those from IC neurons are smaller than ones from lower brainstem sources (Ito et al, ; Ito & Oliver, ). In the Japanese house bat, LG neurons in the ICCd received smaller terminals than those in the ICCvm (Figure ), suggesting that the main sources of axosomatic excitatory inputs on ICCd LG neurons are local and commissural IC neurons, while those on ICCvm LG neurons are the DCN, SOC, and ILL. As LG neurons are GABAergic and send axons locally (Ito et al, ), LG cells may be driven by the onset response of IC neurons and, in turn, may inhibit local neurons. If the information of the onset of an FM pulse, which has a higher frequency component than the terminal phase, arrives at an LG soma faster than in neurons that receive inputs from the LG neuron, inhibition from the LG neuron will suppress the onset response and result in a longer latency.…”

“…LG cells receive converged inputs from ascending fibers from lower brainstem neurons (Ito et al, ) and collaterals from local neurons (Ito & Oliver, ). Furthermore, in echolocating bat, LG, and glutamatergic cells receive input from distant part of the IC, while SG cells receive input from their proximity (Ito, Furuyama, Hase, Kobayasi, & Hiryu, ). These findings suggest that LG cells are suitable for sound information integration.…”

Inhibitory Neural Circuits in the Mammalian Auditory Midbrain

“…Thus, the ascending inhibitory inputs to the mammalian IC are both GABAergic and glycinergic. In addition to these inhibitory inputs from the brainstem, it was anatomically verified that the neurons in the mammalian IC received inhibitory inputs from both the ipsilateral 123 and contralateral sides. 52,53…”

“…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.…”

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.…”