Comparative Physiology of Sound Localization in Four Species of Owls (Part 1 of 2)

Bilateral ear asymmetry is found in some, but not all, species of owls. We investigated the neural basis of sound localization in symmetrical and asymmetrical species, to deduce how ear asymmetry might have evolved from the ancestral condition, by comparing the response properties of neurons in the external nucleus of the inferior colliculus (ICx) of the symmetrical burrowing owl and asymmetrical long-eared owl with previous findings in the symmetrical great horned owl and asymmetrical barn owl. In the ICx of all of these owls, the neurons had spatially restricted receptive fields, and auditory space was topographically mapped. In the symmetrical owls, ICx units were not restricted in elevation, and only azimuth was mapped in ICx. In the barn owl, the space map is two-dimensional, with elevation forming the second dimension. Receptive fields in the long-eared owl were somewhat restricted in elevation, but their tuning was not sharp enough to determine if elevation is mapped. In every species, the primary cue for azimuth was interaural time difference, although ICx units were also tuned for interaural intensity difference (IID). In the barn owl, the IIDs of sounds with frequencies between about 5 and 8 kHz vary systematically with elevation, and the IID selectivity of ICx neurons primarily encodes elevation. In the symmetrical owls, whose ICx neurons do not respond to frequencies above about 5 kHz, IID appears to be a supplementary cue for azimuth. We hypothesize that ear asymmetry can be exploited by owls that have evolved the higher-frequency hearing necessary to generate elevation cues. Thus, the IID selectivity of ICx neurons in symmetrical owls may preadapt them for asymmetry; the neural circuitry that underlies IID selectivity is already present in symmetrical owls, but because IID is not absolutely required to encode azimuth it can come to encode elevation in asymmetrical owls.