Differences in the neural representation of binaural sound localization cues in the auditory midbrain of chicken and barn owl

Abstract

The sound localisation behaviour of the nocturnally hunting barn owl and its underlying neural computations is a textbook example of neuroethology. Differences in sound timing and level at the two ears are integrated in a series of well characterised steps, from brainstem to inferior colliculus, resulting in a topographical neural representation of auditory space. It remains an important question of brain evolution how this specialised case derived from a more plesiomorphic pattern. The present study is the first to match physiology and anatomical subregions in the non-owl avian inferior colliculus. Single-unit responses in the chicken inferior colliculus were tested for selectivity to different frequencies and to the binaural difference cues. Their anatomical origin was reconstructed with the help of electrolytic lesions and immunohistochemical identification of different subregions of the inferior colliculus, based on previous characterisations in owl and chicken. In contrast to barn owl, there was no distinct differentiation of responses in the different subregions. We found neural topographies for both binaural cues but no evidence for a coherent representation of auditory space. The results are consistent with previous work in pigeon inferior colliculus and chicken higher-order midbrain and suggest a plesiomorphic condition of multisensory integration in the midbrain that is dominated by lateral panoramic vision.