Two Types of Auditory Spatial Receptive Fields in Different Parts of the Chicken's Midbrain.

Abstract

The optic tectum (OT) is an avian midbrain structure involved in the integration of visual and auditory stimuli. Studies in the barn owl, an auditory specialist, have shown that spatial auditory information is topographically represented in the OT. Little is known about how auditory space is represented in the midbrain of birds with generalist hearing, i.e., most of avian species lacking peripheral adaptations such as facial ruffs or asymmetric ears. Thus, we conducted in vivo extracellular recordings of single neurons in the OT and in the external portion of the formatio reticularis lateralis (FRLx), a brain structure located between the inferior colliculus (IC) and the OT, in anaesthetized chickens of either sex. We found that most of the auditory spatial receptive fields (aSRFs) were spatially confined both in azimuth and elevation, divided into two main classes: round aSRFs, mainly present in the OT, and annular aSRFs, with a ring-like shape around the interaural axis, mainly present in the FRLx. Our data further indicate that interaural time difference (ITD) and interaural level difference (ILD) play a role in the formation of both aSRF classes. These results suggest that, unlike mammals and owls which have a congruent representation of visual and auditory space in the OT, generalist birds separate the computation of auditory space in two different midbrain structures. We hypothesize that the FRLx-annular aSRFs define the distance of a sound source from the axis of the lateral visual fovea, whereas the OT-round aSRFs are involved in multimodal integration of the stimulus around the lateral fovea.SIGNIFICANCE STATEMENT Previous studies implied that auditory spatial receptive fields (aSRFs) in the midbrain of generalist birds are only confined along azimuth. Interestingly, we found SRFs s in the chicken to be confined along both azimuth and elevation. Moreover, the auditory receptive fields are arranged in a concentric manner around the overlapping interaural and visual axes. These data suggest that in generalist birds, which mainly rely on vision, the auditory system mainly serves to align auditory stimuli with the visual axis, while auditory specialized birds like the barn owl compute sound sources more precisely and integrate sound positions in the multimodal space map of the optic tectum (OT).