Principal cells of the brainstem's interaural sound level detector are temporal differentiators rather than integrators.

Tom P Franken,Philip X Joris,Philip H Smith

doi:10.7554/elife.33854

Tom P Franken, Philip X Joris + Show 1 more

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https://doi.org/10.7554/elife.33854

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Journal: eLife	Publication Date: Jun 14, 2018
Citations: 52	License type: CC BY 4.0

Affiliation: KU Leuven, University of Wisconsin–Madison

Abstract

The brainstem's lateral superior olive (LSO) is thought to be crucial for localizing high-frequency sounds by coding interaural sound level differences (ILD). Its neurons weigh contralateral inhibition against ipsilateral excitation, making their firing rate a function of the azimuthal position of a sound source. Since the very first in vivo recordings, LSO principal neurons have been reported to give sustained and temporally integrating 'chopper' responses to sustained sounds. Neurons with transient responses were observed but largely ignored and even considered a sign of pathology. Using the Mongolian gerbil as a model system, we have obtained the first in vivo patch clamp recordings from labeled LSO neurons and find that principal LSO neurons, the most numerous projection neurons of this nucleus, only respond at sound onset and show fast membrane features suggesting an importance for timing. These results provide a new framework to interpret previously puzzling features of this circuit.

Highlights

The lateral superior olive (LSO) in the superior olivary complex is a major component of the brainstem high-frequency sound localization circuitry
Neurons in the LSO accomplish this by weighing the sound input to the ipsilateral ear, conveyed via an excitatory projection from the ipsilateral cochlear nucleus (Cant, 1991; Smith et al, 1993; Doucet and Ryugo, 2003), against the sound input to the contralateral ear, conveyed via an inhibitory afferent from the homolateral medial nucleus of the trapezoid body (Figure 1A) (Glendenning et al, 1985; Banks and Smith, 1992; Sommer et al, 1993). This process results in firing rates that vary monotonically with interaural sound level differences (ILD), and this tuning is conveyed to targets in the midbrain: the ipsilateral and contralateral inferior colliculi (IC) and the contralateral dorsal nucleus of the lateral lemniscus (DNLL) (Glendenning and Masterton, 1983; Moore, 1988; Saint Marie et al, 1989; Glendenning et al, 1992)
We present the first evidence that all these cell types are excited by sounds to the ipsilateral ear and inhibited by sounds to the contralateral ear, and that they conform to the tonotopic LSO map

Summary

Introduction

The lateral superior olive (LSO) in the superior olivary complex is a major component of the brainstem high-frequency sound localization circuitry. Neurons in the LSO accomplish this by weighing the sound input to the ipsilateral ear, conveyed via an excitatory (glutamatergic) projection from the ipsilateral cochlear nucleus (Cant, 1991; Smith et al, 1993; Doucet and Ryugo, 2003), against the sound input to the contralateral ear, conveyed via an inhibitory (glycinergic) afferent from the homolateral medial nucleus of the trapezoid body (Figure 1A) (Glendenning et al, 1985; Banks and Smith, 1992; Sommer et al, 1993) This process results in firing rates that vary monotonically with ILD, and this tuning is conveyed to targets in the midbrain: the ipsilateral and contralateral inferior colliculi (IC) and the contralateral dorsal nucleus of the lateral lemniscus (DNLL) (Glendenning and Masterton, 1983; Moore, 1988; Saint Marie et al, 1989; Glendenning et al, 1992). This feature is used as a physiological criterion to define LSO units (e.g. Finlayson and Caspary, 1989; Joris and Yin, 1995; Tollin et al, 2008; Tsai et al, 2010)

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