Benefits of Enhanced Phase-Locking for Binaural Coding of Amplitude-Modulated Sounds

The neural processing of interaural time and level differences (ITDs/ILDs) underlies binaural sound localization. Neurons of the mammalian lateral superior olive (LSO) are sensitive to ILDs and envelope-ITDs of acoustic stimuli. Bushy cells in the anteroventral cochlear nucleus convey relevant information from auditory nerve (AN) fibers to the LSO. More specifically, spherical bushy cells (SBCs) send ipsilateral excitatory inputs, while globular bushy cells (GBCs) project to the contralateral medial nucleus of the trapezoid body that provides inhibitory inputs to the LSO. Previous studies in vivo reported an enhancement of phase-locking in bushy cells compared to AN. This enhancement has been hypothesized to benefit temporal coding in binaural neurons, but its actual contribution in LSO remains unclear. Here we investigate this question by computational modeling of binaural circuity incorporating the AN, SBC/GBC, and LSO stages. Both bushy cell models were calibrated to replicate known physiological responses, including the representative peristimulus time histograms for high-frequency tones and enhanced phase-locking to low-frequency envelopes. We then simulated the binaural tuning of LSO with and without the bushy cell stage. The synaptic inputs to the LSO model were adjusted so that the simulated ILD-tuning remains unaltered between the input configurations. By adding the bushy cell stage, the simulated binaural response of LSO became more sharply tuned for envelope-ITDs. Furthermore, the envelope-ITD sensitivity was extended up to around 600 Hz, matching previously observed physiological limits. These results provide computational evidence for the functional benefit of having bushy cells in the binaural sound localization circuit.