The neural coding of auditory space

Abstract

The barn owl's auditory system computes interaural differences in time and amplitude and derives from them the horizontal and vertical coordinates of the sound source, respectively. Within the external nucleus of its inferior colliculus are auditory neurones, called 'space-specific neurones', that have spatial receptive fields. To activate a space-specific neurone, a sound must originate from a circumscribed region of space, or, if the sounds are delivered to each ear separately, using earphones, the stimuli must have the combination of interaural time and amplitude difference that simulates a sound broadcast from their receptive field. The sound-localization cues are processed in parallel, non-overlapping pathways extending from the cochlear nuclei to the subdivision of the inferior colliculus that innervates the space-specific neurones. Processing in the time pathway involves the coding of monaural phase angle, the derivation of sensitivity for interaural phase difference, and the calculation of interaural time difference (ITD) from interaural phase difference. The last process involves groups of neurones in the inferior colliculus whose collective firing signals a unique ITD, even though the activity of each constituent neurone signals multiple ITDs. The projections of these ensembles to the space-specific neurone endow the latter with a selectivity for ITD. Processing in the amplitude channel, about which less is known, initially involves an inhibitory process that sharpens the directional sensitivity of neurones in a lateral lemniscal nucleus. The inhibition is mediated by a commissural projection from the same lemniscal nucleus of the opposite side. At higher levels of the auditory system, neurones that are tuned to a limited range of interaural amplitude differences are found. It is proposed that at these higher stages, interaural amplitude difference, like ITD, is coded amidst an ensemble of neurones.