Abstract

The auditory system relies on temporal precise information transfer, requiring an interplay of synchronously activated inputs and rapid postsynaptic integration. During late postnatal development synaptic, biophysical, and morphological features change to enable mature auditory neurons to perform their appropriate function. How the number of minimal required input fibers and the relevant EPSC time course integrated for action potential generation changes during late postnatal development is unclear. To answer these questions, we used in vitro electrophysiology in auditory brainstem structures from pre-hearing onset and mature Mongolian gerbils of either sex. Synaptic and biophysical parameters changed distinctively during development in the medial nucleus of the trapezoid body (MNTB), the medial superior olive (MSO), and the ventral and dorsal nucleus of the lateral lemniscus (VNLL and DNLL). Despite a reduction in input resistance in most cell types, all required fewer inputs in the mature stage to drive action potentials. Moreover, the EPSC decay time constant is a good predictor of the EPSC time used for action potential generation in all nuclei but the VNLL. Only in MSO neurons, the full EPSC time course is integrated by the neuron’s resistive element, while otherwise, the relevant EPSC time matches only 5–10% of the membrane time constant, indicating membrane charging as a dominant role for output generation. We conclude, that distinct developmental programs lead to a general increase in temporal precision and integration accuracy matched to the information relaying properties of the investigated nuclei.

Highlights

  • Neurons in the auditory brainstem form specialized structure-function relationships

  • In all nuclei the τmem accelerated during late postnatal development (VNLL: p = 0.00039; medial nucleus of the trapezoid body (MNTB): p = 0.019; medial superior olive (MSO): p = 0.00002; dorsal nucleus of the lateral lemniscus (DNLL): p = 0.0001, Mann–Whitney U)

  • The fastest τmem was observed in the MSO (0.236 ms) and the slowest in the DNLL (7.423 ms), while ventral nucleus of the lateral lemniscus (VNLL) and MNTB neurons displayed an intermediate τmem (2.658 and 2.234 ms, respectively, Figure 2B, top)

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Summary

Introduction

Neurons in the auditory brainstem form specialized structure-function relationships. To accommodate their individual functions, neurons refine their biophysical and synaptic properties during postnatal development in a distinct manner. Neurons of the medial superior olive (MSO) for example act as ultra-fast coincidence detectors integrating binaural time differences (Goldberg and Brown, 1969; Yin and Chan, 1990). Neurons of the dorsal nucleus of the lateral lemniscus (DNLL) integrate over longer time windows to generate a long-lasting suppression acting as a temporal binaural filter (Yang and Pollak, 1994; Pecka et al, 2007; Meffin and Grothe, 2009; Siveke et al, 2019). The large glutamatergic somatic synapses in the medial nucleus of the trapezoid body (MNTB; Held, 1893; Forsythe, 1994) and the ventral nucleus of the lateral lemniscus (VNLL; Stotler, 1953; Adams, 1997; Berger et al, 2014) allow for rapid and temporally precise feed-forward inhibition

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