The lateral superior olive in the mouse: Two systems of projecting neurons

Isabella R Williams; Anastasia Filimontseva; Catherine J Connelly; David K Ryugo

doi:10.3389/fncir.2022.1038500

The lateral superior olive in the mouse: Two systems of projecting neurons

Front Neural Circuits. 2022 Oct 20:16:1038500. doi: 10.3389/fncir.2022.1038500. eCollection 2022.

Authors

Isabella R Williams^{1

2}, Anastasia Filimontseva¹, Catherine J Connelly^{1

2}, David K Ryugo^{1

2

3}

Affiliations

¹ Garvan Institute of Medical Research, Darlinghurst, NSW, Australia.
² School of Medical Sciences, University of New South Wales, Kensington, NSW, Australia.
³ Department of Otolaryngology-Head, Neck and Skull Base Surgery, St. Vincent's Hospital, Darlinghurst, NSW, Australia.

Abstract

The lateral superior olive (LSO) is a key structure in the central auditory system of mammals that exerts efferent control on cochlear sensitivity and is involved in the processing of binaural level differences for sound localization. Understanding how the LSO contributes to these processes requires knowledge about the resident cells and their connections with other auditory structures. We used standard histological stains and retrograde tracer injections into the inferior colliculus (IC) and cochlea in order to characterize two basic groups of neurons: (1) Principal and periolivary (PO) neurons have projections to the IC as part of the ascending auditory pathway; and (2) lateral olivocochlear (LOC) intrinsic and shell efferents have descending projections to the cochlea. Principal and intrinsic neurons are intermixed within the LSO, exhibit fusiform somata, and have disk-shaped dendritic arborizations. The principal neurons have bilateral, symmetric, and tonotopic projections to the IC. The intrinsic efferents have strictly ipsilateral projections, known to be tonotopic from previous publications. PO and shell neurons represent much smaller populations (<10% of principal and intrinsic neurons, respectively), have multipolar somata, reside outside the LSO, and have non-topographic, bilateral projections. PO and shell neurons appear to have widespread projections to their targets that imply a more diffuse modulatory function. The somata and dendrites of principal and intrinsic neurons form a laminar matrix within the LSO and share quantifiably similar alignment to the tonotopic axis. Their restricted projections emphasize the importance of frequency in binaural processing and efferent control for auditory perception. This study addressed and expanded on previous findings of cell types, circuit laterality, and projection tonotopy in the LSO of the mouse.

Keywords: anatomy; auditory; isofrequency; lateral superior olive; olivocochlear efferents; tonotopy; topography.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Auditory Pathways / physiology
Inferior Colliculi* / physiology
Mammals
Mice
Neurons
Olivary Nucleus
Superior Olivary Complex*

Grants and funding

This work was made possible by the following funding sources: NHMRC Grant 1080652 to DKR and a bequest from Helen Morgan and donations to the Hearing Research Lab from Charlene and Graham Bradley, Sue and Haydn Daw, and Alan and Lynn Rydge. CJC was recipient of a University International Postgraduate Award from the UNSW Australia. The donors had no role in the direction, analysis, or publication of this work.