Abstract
The medial superior olive (MSO) senses microsecond differences in the coincidence of binaural signals, a critical cue for detecting sound location along the azimuth. An important component of this circuit is provided by inhibitory neurons of the medial and lateral nuclei of the trapezoid body (MNTB and LNTB, respectively). While MNTB neurons are fairly well described, little is known about the physiology of LNTB neurons. Using whole cell recordings from gerbil brainstem slices, we found that LNTB and MNTB neurons have similar membrane time constants and input resistances and fire brief action potentials, but only LNTB neurons fire repetitively in response to current steps. We observed that LNTB neurons receive graded excitatory and inhibitory synaptic inputs, with at least some of the latter arriving from other LNTB neurons. To address the relative timing of inhibition to the MSO from the LNTB versus the MNTB, we examined inhibitory responses to auditory nerve stimulation using a slice preparation that retains the circuitry from the auditory nerve to the MSO intact. Despite the longer physical path length of excitatory inputs driving contralateral inhibition, inhibition from both pathways arrived with similar latency and jitter. An analysis of paired whole cell recordings between MSO and MNTB neurons revealed a short and reliable delay between the action potential peak in MNTB neurons and the onset of the resulting IPSP (0.55 ± 0.01 ms, n = 4, mean ± SEM). Reconstructions of biocytin-labeled neurons showed that MNTB axons ranged from 580 to 858 μm in length (n = 4). We conclude that while both LNTB and MNTB neurons provide similarly timed inhibition to MSO neurons, the reliability of inhibition from the LNTB at higher frequencies is more constrained relative to that from the MNTB due to differences in intrinsic properties, the strength of excitatory inputs, and the presence of feedforward inhibition.
Highlights
To identify the origin of low frequency sounds in the azimuthal plane, animals discern microsecond-order differences in the arrival times of sounds at the two ears
We investigated the intrinsic physiology of lateral nucleus of the trapezoid body (LNTB) neurons and compared it to that of medial nucleus of the trapezoid body (MNTB) neurons
We investigated how LNTB and MNTB neurons are adapted for their roles in sound localization, providing the first descriptions of the intrinsic physiology of LNTB neurons www.frontiersin.org and the first recordings from synaptically coupled pairs of MNTB and medial superior olive (MSO) neurons
Summary
To identify the origin of low frequency sounds in the azimuthal plane, animals discern microsecond-order differences in the arrival times of sounds at the two ears. Neurons in the medial superior olive (MSO) detect these interaural time differences (ITDs) by comparing the timing of excitatory inputs received from pathways that begin at the ipsilateral and contralateral cochlea (Figure 1A; Joris and Yin, 2007; Grothe et al, 2010). LNTB and MNTB neurons are glycinergic (Adams and Mugnaini, 1990; Spirou and Berrebi, 1997), and receive excitatory input from globular bushy cells in the ipsilateral and contralateral cochlear nuclei, respectively (Figure 1A; Tolbert et al, 1982; Friauf and Ostwald, 1988; Kuwabara et al, 1991; Smith et al, 1991; Thompson and Schofield, 2000). In the in vitro slice preparation, stimulation of LNTB or MNTB inputs elicits fast inhibitory responses in MSO neurons (Grothe and Sanes, 1993, 1994; Magnusson et al, 2005; Chirila et al, 2007; Couchman et al, 2010; Fischl et al, 2012)
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