Auditory tuning for spatial cues in the barn owl basal ganglia

Abstract

1. The basal ganglia are known to contribute to spatially guided behavior. In this study, we investigated the auditory response properties of neurons in the barn owl paleostriatum augmentum (PA), the homologue of the mammalian striatum. The data suggest that the barn owl PA is specialized to process spatial cues and, like the mammalian striatum, is involved in spatial behavior. 2. Single- and multiunit sites were recorded extracellularly in ketamine-anesthetized owls. Spatial receptive fields were measured with a free-field sound source, and tuning for frequency and interaural differences in timing (ITD) and level (ILD) was assessed using digitally synthesized dichotic stimuli. 3. Spatial receptive fields measured at nine multiunit sites were tuned to restricted regions of space: tuning widths at half-maximum response averaged 22 +/- 9.6 degrees (mean +/- SD) in azimuth and 54 +/- 22 degrees in elevation. 4. PA sites responded strongly to broadband sounds. When frequency tuning could be measured (n = 145/201 sites), tuning was broad, averaging 2.7 kHz at half-maximum response, and tended to be centered near the high end of the owl's audible range. The mean best frequency was 6.2 kHz. 5. All PA sites (n = 201) were selective for both ITD and ILD. ITD tuning curves typically exhibited a single, large “primary” peak and often smaller, “secondary” peaks at ITDs ipsilateral and/or contralateral to the primary peak. Three indices quantified the selectivity of PA sites for ITD. The first index, which was the percent difference between the minimum and maximum response as a function of ITD, averaged 100 +/- 29%. The second index, which represented the size of the largest secondary peak relative to that of the primary peak, averaged 49 +/- 23%. The third index, which was the width of the primary ITD peak at half-maximum response, averaged only 66 +/- 35 microseconds. 6. The majority (96%; n = 192/201) of PA sites were tuned to a single “best” value of ILD. The widths of ILD tuning curves at half-maximum response averaged 24 +/- 9 dB. 7. On average, sound level had no effect on a site's best ITD or best ILD nor did it affect ITD tuning widths. ILD tuning widths did, however, tend to increase slightly with sound level (average effect was 0.1 dB ILD/dB). 8. Most PA sites responded best to contralateral-ear leading ITDs with a majority being tuned to ITDs near 0 microsecond (corresponding to sound-source locations just contralateral to the midline).(ABSTRACT TRUNCATED AT 400 WORDS)