Local and commissural IC neurons make axosomatic inputs on large GABAergic tectothalamic neurons

Abstract

Large GABAergic (LG) neurons are a distinct type of neuron in the inferior colliculus (IC) identified by their dense VGLUT2-containing axosomatic synaptic terminals. Yet, the sources of these terminals are unknown. Since IC glutamatergic neurons express VGLUT2, and IC neurons are known to have local collaterals, we tested the hypothesis that these excitatory, glutamatergic axosomatic inputs on LG neurons come from local axonal collaterals and commissural IC neurons. We injected a recombinant viral tracer into the IC which enabled Golgi-like GFP labeling in both dendrites and axons. In all cases, we found terminals positive for both GFP and VGLUT2 (GFP+/VGLUT2+) that made axosomatic contacts on LG neurons. One to six axosomatic contacts were made on a single LG cell body by a single axonal branch. The GFP-labeled neurons giving rise to the VGLUT2+ terminals on LG neurons were close by. The density of GFP+/VGLUT2+ terminals on the LG neurons was related to the number of nearby GFP-labeled cells. On the contralateral side, a smaller number of LG neurons received axosomatic contacts from GFP+/VGLUT2+ terminals. In cases with a single GFP-labeled glutamatergic neuron, the labeled axonal plexus was flat, oriented in parallel to the fibrodendritic laminae, and contacted 9–30 LG cell bodies within the plexus. Our data demonstrated that within the IC microcircuitry, there is a convergence of inputs from local IC excitatory neurons on LG cell bodies. This suggests that LG neurons are heavily influenced by the activity of the nearby laminar glutamatergic neurons in the IC.

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

“…It is also noted that synaptic domains are interconnected by LG neurons as well as glutamatergic interneurons (Ito & Oliver, 2014). The computation made in each synaptic domain would be modified by the interconnection of LG and GLU cells.…”

“…Furthermore, information conveyed by interconnecting LG and GLU cells is likely to be different since both cell types receive different combination of extrinsic inputs (Chen, Cheng, Ito, & Song, 2018) and LG cells receive inputs from GLU cells in different synaptic domains (Ito & Oliver, 2014). Based on studies on rodents, LG neurons integrate information from multiple brainstem nuclei, while GLU cells integrate inputs related to their synaptic domains (Chen et al., 2018; Ito & Oliver, 2014; Ito et al., 2015). Therefore, it is suggested that LG cells control the entire IC circuit according to global state of brainstem nuclei, while GLU cells control according to the state of specific pathways.…”

The auditory corticocollicular system: Molecular and circuit-level considerations

“…Other possible explanations exist. For example, given the demonstration that local collaterals from CNIC neurons branch to innervate large GABAergic neurons throughout the IC (Ito and Oliver 2014), stimulation of the LC may cause antidromic activation of CNIC neurons that project to the LC. This may have activated local GABAergic neurons, producing the above-described inhibition in the Jen et al study.…”

Convergence of lemniscal and local excitatory inputs on large GABAergic tectothalamic neurons

“…cochlear nuclei (CN), superior olivary complex (SOC), and nuclei of the lateral lemniscus (NLL). In addition to the ascending lemniscal inputs, neighboring neurons in IC will influence each other since most IC neurons have local collaterals (Ito and Oliver, 2014; Oliver et al, 1991; Wallace et al, 2012). However, direct morphological evidence for the convergence of ascending and local inputs is lacking.…”