Abstract
The integration of excitatory and inhibitory synaptic inputs is fundamental to neuronal processing. In the mammalian auditory brainstem, neurons compare excitatory and inhibitory inputs from the ipsilateral and contralateral ear, respectively, for sound localization. However, the temporal precision and functional roles of inhibition in this integration process are unclear. Here, we demonstrate by in vivo recordings from the lateral superior olive (LSO) that inhibition controls spiking with microsecond precision throughout high frequency click trains. Depending on the relative timing of excitation and inhibition, neuronal spike probability is either suppressed or—unexpectedly—facilitated. In vitro conductance-clamp LSO recordings establish that a reduction in the voltage threshold for spike initiation due to a prior hyperpolarization results in post-inhibitory facilitation of otherwise sub-threshold synaptic events. Thus, microsecond-precise differences in the arrival of inhibition relative to excitation can facilitate spiking in the LSO, thereby promoting spatial sensitivity during the processing of faint sounds.
Highlights
The integration of excitatory and inhibitory synaptic inputs is fundamental to neuronal processing
During binaurally presented click-trains, the response rates of the same neuron were clearly modulated by the composite timing delays” (cTDs), i.e., the relative timing of the inputs from the two ears (Fig. 1f, righthand panel)
We focused our analysis on the “best ICI” of each neuron, i.e., the ICI that elicited maximal response rate modulation as a function of cTD
Summary
The integration of excitatory and inhibitory synaptic inputs is fundamental to neuronal processing. This processing motif is prominent in auditory brainstem circuits dedicated to the processing of binaural cues for the localization of sound sources (Fig. 1a)[7,13,14,15] In mammals, these cues are the interaural level and time differences (ILD and ITD, respectively) and are first computed by neurons in the lateral and the medial superior olive (LSO and MSO, respectively)[16,17]. These cues are the interaural level and time differences (ILD and ITD, respectively) and are first computed by neurons in the lateral and the medial superior olive (LSO and MSO, respectively)[16,17] In both nuclei, the computation is based on precise interactions of glutamatergic excitation and glycinergic inhibition in response to sounds arriving at the two ears[15,16,18,19] (Fig. 1b, c). Because first-spike latencies can vary by ~1 ms/10 dB any change in the location of a sound source (e.g., from the ispilateral to the contralateral hemisphere) can cause shifts in the relative timing of inhibition and excitation in the range of many hundreds of μs[7,33]
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