Microsecond interaural time differences of acoustic transients are decoded by inhibitory-excitatory interactions in neurons of the lateral superior olive

Abstract

The lateral superior olive (LSO) in the auditory brainstem generates sensitivity to interaural level differences (ILD), an important cue for sound localization, by comparing excitatory (E) input from the ipsilateral ear with inhibitory (I) input from the contralateral ear. Large axosomatic synapses (e.g., calyx of Held) point to the importance of precise temporal processing, but that is not easily reconciled with ILD detection. We propose that the IE interaction allows detection of interaural time differences (ITD) of acoustic transients, to which humans are exquisitely sensitive. We obtained in vivo whole cell recordings of LSO and MSO neurons in the gerbil, while presenting monaural and binaural clicks. We found that ITD functions to clicks in the LSO are surprisingly steep, in contrast to MSO neurons, which are considered the main ITD detectors. Intracellular LSO recordings show EPSPs generated by the ipsilateral click and IPSPs by the contralateral click, where IPSPs often arrive earlier. Binaural spiking is maximally suppressed when the EPSP coincides with the falling slope rather than the peak of the IPSP. We conclude that LSO neurons are more sensitive to ITDs of transients than MSO neurons. This clarifies the importance of timing specializations in the LSO circuit.