A Dominance Hierarchy of Auditory Spatial Cues in Barn Owls Ilana B. Witten, Phyllis F. Knudsen, Eric I. Knudsen* Neurobiology Department, Stanford University Medical Center, Stanford, California, United States of America Abstract Background: Barn owls integrate spatial information across frequency channels to localize sounds in space. Methodology/Principal Findings: We presented barn owls with synchronous sounds that contained different bands of frequencies (3–5 kHz and 7–9 kHz) from different locations in space. When the owls were confronted with the conflicting localization cues from two synchronous sounds of equal level, their orienting responses were dominated by one of the sounds: they oriented toward the location of the low frequency sound when the sources were separated in azimuth; in contrast, they oriented toward the location of the high frequency sound when the sources were separated in elevation. We identified neural correlates of this behavioral effect in the optic tectum (OT, superior colliculus in mammals), which contains a map of auditory space and is involved in generating orienting movements to sounds. We found that low frequency cues dominate the representation of sound azimuth in the OT space map, whereas high frequency cues dominate the representation of sound elevation. Conclusions/Significance: We argue that the dominance hierarchy of localization cues reflects several factors: 1) the relative amplitude of the sound providing the cue, 2) the resolution with which the auditory system measures the value of a cue, and 3) the spatial ambiguity in interpreting the cue. These same factors may contribute to the relative weighting of sound localization cues in other species, including humans. Citation: Witten IB, Knudsen PF, Knudsen EI (2010) A Dominance Hierarchy of Auditory Spatial Cues in Barn Owls. PLoS ONE 5(4): e10396. doi:10.1371/ journal.pone.0010396 Editor: Andrew Iwaniuk, University of Lethbridge, Canada Received October 25, 2009; Accepted March 22, 2010; Published April 28, 2010 Copyright: 2010 Witten et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the National Institutes of Health (NIH) and National Science Foundation (NSF) graduate research fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: eknudsen@stanford.edu Introduction The central auditory system infers the location of a sound source in space by evaluating and combining a variety of cues. The dominant localization cues are binaural cues, based on interaural level differences (ILD) and interaural timing differences (ITD), the latter based on measurements of interaural phase differences (IPD) [1]. Because the correspondence between values of ITD and ILD and locations in space varies with the frequency of the sound, the auditory system measures these cues in frequency-specific channels and evaluates them in a frequency-specific manner. The information provided by these cues is combined to create a representation of the most likely location of the acoustic stimulus. Human psychophysical studies, in which localization cues from different frequencies are put into conflict, demonstrate that these frequency-specific sound localization cues are weighted differen- tially in determining the location of a sound source. For example, when humans are presented with simultaneous low frequency (500 Hz, 1 kHz or 2 kHz) and high frequency (4 kHz) sounds from different locations, the high frequency sound is grouped perceptually with the low frequency sound (because the sounds are synchronized [2]), and the combined stimulus is lateralized near the position of the low frequency source [3]. In other experiments, low frequency sounds have been shown to alter the lateralization of synchronous high frequency sounds, but not vice versa [4,5]. These results indicate that the human auditory system follows the rule that low frequency localization cues dominate over high frequency cues when localizing a sound source. The basis for the dominance of low over high frequency cues is thought to be related to the relative spatial resolution provided by each cue. The discriminability index (d’), measured psychophysically as the ability to judge whether a sound originates from the left or right of the midline, predicts the relative dominance of localization cues when different frequency components containing conflicting cues are presented simultaneously [5,6]. We looked for evidence of an analogous dominance hierarchy among sound localization cues in barn owls, and we explored underlying factors that could account for their relative dominance. Owls exploit the same binaural cues for localizing sounds as do humans. However, the human auditory system is only able to measure IPDs for frequencies up to about 1.3 kHz [7,8] whereas, the barn owl auditory system measures IPD cues up to about 8 kHz [9]. In addition, the barn owl’s external ears are asymmetrical which causes the left ear to be more sensitive to high frequency sounds (.3 kHz) from below and the right ear to be more sensitive to high frequency sounds from above [10]. The ear asymmetry causes the ILDs of frequencies above 3 kHz to vary with the elevation of a sound source. Thus, each frequency above 3 kHz provides two binaural cues: an IPD cue that varies with azimuth and an ILD cue that varies primarily with elevation [11]. PLoS ONE | www.plosone.org 1 April 2010 | Volume 5 | Issue 4 | e10396