Learning to localize sounds like a barn owl

Abstract

O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=91 SRC="FIGDIR/small/704341v2_ufig1.gif" ALT="Figure 1"> View larger version (29K): org.highwire.dtl.DTLVardef@1d6092dorg.highwire.dtl.DTLVardef@f48c26org.highwire.dtl.DTLVardef@11d1f96org.highwire.dtl.DTLVardef@104e1a2_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOGraphical abstractC_FLOATNO Giving humans asymmetric barn-owl-like ears disrupts elevation localization by removing normal spectral pinna cues. With experience, listeners partially relearn to localize elevation using novel binaural cues. Results show that adult auditory spatial processing is flexible enough to repurpose cues, but strongly constrained in the extent of relearning. C_FIG The brain computes sound location from auditory spatial cues. Humans and barn owls both localize sounds accurately, yet they rely on fundamentally different cue configurations shaped by their ear anatomy and neural circuitry. In humans, symmetrical ears provide interaural time and level differences (ITD and ILD) for horizontal localization, while vertical localization depends primarily on high-frequency, monaural spectral cues generated by the pinnae. Barn owls, by contrast, possess asymmetrical ears and use binaural cues for both azimuth and elevation. Because auditory pathways are tuned to species-specific cue statistics, it remains unclear whether humans can adapt when binaural level cues are also made informative about elevation. We tested this by fitting human listeners with asymmetric ear molds that disrupted normal spectral cues, introduced elevation-dependent ILDs, and left ITDs unaffected. Participants wore the molds during daily life and were tested with broadband, high-pass, and low-pass noise bursts. Acute mold exposure severely degraded elevation localization, whereas horizontal localization remained largely unaffected. With prolonged exposure, elevation localization improved, but adaptation was limited, variable across listeners, and fluctuated across sessions. Improvement was strongest for broadband sounds. Because broadband and high-pass sounds both contained high-frequency information, this broadband advantage cannot be explained by access to additional spectral cues alone. Instead, it suggests that low-frequency ITDs helped listeners exploit the altered binaural cue structure, including the elevation-dependent ILDs introduced by the molds. These findings show that humans can partially adapt to asymmetric outer-ear acoustics when complementary spatial cues help resolve ambiguity in the altered cue structure.