Dissection of the contribution of bushy cell delays to sound localization in juvenile and adult Mongolian gerbils

Abstract

Sound sources along the azimuth generate interaural time differences in arrival (ITDs) at the ears. According to Jeffress hypothesis, ITDs are detected by coincidence-sensitive neurons of the medial superior olive (MSO) for which a differential axonal delay from each ear to the MSO compensates for the ITDs. The origin and development of these delays remain poorly understood. To this end, we made recordings from bushy cells (BCs), which project to both MSOs, in adult and in 2-4-week-old Mongolian gerbils of either sex. First spike latency revealed a frequency-dependent delay likely originating in the cochlea. Latencies were markedly larger for pure tone stimulation than for complex sounds. Combined with our published recordings from the MSO, we observed a developmental decrease in most delays, including the contralateral BC-to-MSO axonal delay. Unexpectedly, the ipsilateral BC-to-MSO axonal delay did not decrease. Anatomical brainstem reconstructions revealed that the inter-MSO distance was stable whereas the cochlear nucleus-to-MSO distance increased during development. Together, this indicated an increase in axonal propagation velocity, particularly for the contralateral projection. The variability in the averaged firing onset between BCs was found to be as large as the variance in bITDs, suggesting that BCs with matching firing onset are selected to converge onto the same MSO neuron. Together, our results indicate that the developmental speedup of ear-to-MSO delays contributes greatly to bringing the bITDs within their ecological range, but that the difference in path length is not overcome, keeping the ITD tuning biased to contralateral sound sources.