Processing of Interaural Level Differences in the Auditory Brainstem of the Barn Owl

Abstract

Nervous systems process information about the environment in order to generate adaptive behavior. Sensory information that is obtained through different modalities, gleaned from different interactions of the animal with its surroundings, generated by different neural algorithms, or used to infer different distal stimulus properties, is often processed by distinct pathways in the brain. The auditory system compares sounds at the two ears in order to derive the location of the source. In the barn owl, Tyto alba, this is accomplished by interaural comparisons of the time that a sound reaches each ear, and of the level (intensity) at each ear. Interaural time differences code for horizontal positions of sound sources while interaural level differences, due to a vertical asymmetry in the owl's ears, can encode the vertical position of a sound. These two cues together can assign unique locations to sound sources in space. The barn owl processes time- and level differences in separate neural channels that converge in the inferior colliculus. This structure is the first site of neurons with spatially restricted auditory receptive fields, and with a neural map of auditory space. Downstream projections from here provide the sensory input for accurate sound localization by saccadic head movements. I report that the owl's two auditory processing streams are also segregated histochemically. The pathway that computes level differences stains especially strongly for the enzyme acetylcholinesterase, which may underlay processing of scalar (intensity) information over large dynamic ranges. This staining is complementary to immunohistochemical staining for calbindin, which has been shown previously to stain the pathway that processes interaural time differences. In further hodological and physiological experiments, I describe the algorithms that generate tuned responses in the inferior colliculus that encode vertical sound source position. This study shows that a lemniscal nucleus, nucleus ventralis lemnisci lateralis pars posterior (VLVp), projects bilaterally to a subdivision of the inferior colliculus (the shell of ICc). This projection appears to preserve tonotopy, and to provide inhibition by sounds of large interaural level difference. This probably GABAergic mechanism leads to the synthesis of neuronal responses in the inferior colliculus that are narrowly tuned to interaural level difference. My methodological strategy was to increase or decrease activity in VLVp by injection of blockers or agonists of GABA-A receptors, and then to record downstream in the inferior colliculus any changes in response tuning that resulted. The study suggests that the bilateral inhibition by VLVp is sufficient to explain the peaked responses to level differences of collicular neurons. Excitatory input to the inferior colliculus is conveyed by fibers of the lateral lemniscus, and may arise from a number of stations, including lemniscal and cochlear nuclei. The circuits I describe determine the tuning of cells to interaural level differences, but are independent of and have no effect on the tuning to interaural time differences, and further support that time and level are processed separately in the owl's brainstem.