Commissural Gain Control Enhances the Midbrain Representation of Sound Location

Abstract

Accurate localization of sound sources is essential for survival behavior in many species. The inferior colliculi (ICs) are the first point in the auditory pathway where cues used to locate sounds, ie, interaural time differences (ITDs), interaural level differences (ILDs), and pinna spectral cues, are all represented in the same location. These cues are first extracted separately on each side of the midline in brainstem nuclei that project to the ICs. Because of this segregation, each IC predominantly represents stimuli in the contralateral hemifield. We tested the hypothesis that commissural connections between the ICs mediate gain control that enhances sound localization acuity. We recorded IC neurons sensitive to either ITDs or ILDs in anesthetized guinea pig, before, during, and following recovery from deactivation of the contralateral IC by cryoloop cooling or microdialysis of procaine. During deactivation, responses were rescaled by divisive gain change and additive shifts, which reduced the dynamic range of ITD and ILD response functions and the ability of neurons to signal changes in sound location. These data suggest that each IC exerts multiplicative gain control and subtractive shifts over the other IC that enhances the neural representation of sound location. Furthermore, this gain control operates in a similar manner on both ITD-and ILD-sensitive neurons, suggesting a shared mechanism operates across localization cues. Our findings reveal a novel dependence of sound localization on commissural processing.

A novel class of inferior colliculus principal neurons labeled in vasoactive intestinal peptide-Cre mice

“…The activation of NMDA receptors in our recordings may indicate that excitatory commissural synapses tend to be located on the distal dendrites or dendritic spines of VIP neurons, where the local membrane potential might be sufficiently depolarized by activation of AMPA receptors to remove Mg 2+ block of NMDA receptors. A distal location would be consistent with the proposed modulatory role for commissural inputs (Orton et al, 2016; Orton and Rees, 2014). Similarly, the lack of NMDA receptor activation by DCN afferents might indicate that DCN synapses are located on proximal dendrites or possibly on the soma itself, or that these synapses lack NMDA receptors.…”

Developmental changes in the excitatory short‐term plasticity at input synapses in the rat inferior colliculus

“…In this context, this study may invoke a similar mechanism of excitatory signal integration from the LL‐ and CoIC pathways at CNIC neurons. It has been recently shown that commissural inputs in the IC enhance sound localization in vivo (Orton, Papasavvas, & Rees, ), and present findings may have some functional relevance in the context of sound localization.…”

A Novel Class of Inferior Colliculus Principal Neurons Labeled in Vasoactive Intestinal Peptide-Cre Mice

“…The 410 activation of NMDA receptors in our recordings may indicate that excitatory commissural synapses tend 411 to be located on the distal dendrites or dendritic spines of VIP neurons, where the local membrane 412 potential might be sufficiently depolarized by activation of AMPA receptors to remove Mg 2+ block of 413 NMDA receptors. A distal location would be consistent with the proposed modulatory role for 414 commissural inputs(Orton et al, 2016;Orton and Rees, 2014). Similarly, the lack of NMDA receptor 415 activation by DCN afferents might indicate that DCN synapses are located proximal to the soma, possibly 416 on the soma itself, or that these synapses lack NMDA receptors.…”