Axonal Branching Patterns as Sources of Delay in the Mammalian Auditory Brainstem: A Re-Examination

In models of temporal processing, time delays incurred by axonal propagation of action potentials play a prominent role. A pre-eminent model of temporal processing in audition is the binaural model of Jeffress (1948), which has dominated theories regarding our acute sensitivity to interaural time differences (ITDs). In Jeffress' model, a binaural cell is maximally active when the ITD is compensated by an internal delay, which brings the inputs from left and right ears in coincidence, and which would arise from axonal branching patterns of monaural input fibers. By arranging these patterns in systematic and opposite ways for the ipsilateral and contralateral inputs, a range of length differences, and thereby of internal delays, is created so that the ITD is transformed into a spatial activation pattern along the binaural nucleus. We reanalyze single, labeled, and physiologically characterized axons of spherical bushy cells of the cat anteroventral cochlear nucleus, which project to binaural coincidence detectors in the medial superior olive (MSO). The reconstructions largely confirm the observations of two previous reports, but several features are observed that are inconsistent with Jeffress' model. We found that ipsilateral projections can also form a caudally directed delay line pattern, which would counteract delays incurred by caudally directed contralateral projections. Comparisons of estimated axonal delays with binaural physiological data indicate that the suggestive anatomical patterns cannot account for the frequency-dependent distribution of best delays in the cat. Surprisingly, the tonotopic distribution of the afferent endings indicate that low characteristic frequencies are under-represented rather than over-represented in the MSO.