A Dominance Hierarchy of Auditory Spatial Cues in Barn Owls

University of Lethbridge, Canada
PLoS ONE (Impact Factor: 3.23). 04/2010; 5(4):e10396. DOI: 10.1371/journal.pone.0010396
Source: PubMed


Barn owls integrate spatial information across frequency channels to localize sounds in space.
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.
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.

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    • "Spatial orientation is based on integration of information collected from the surrounding environment with the use of senses. In birds, vision is of primary importance; however, other senses can also play important role (Ioalè et al. 1990; Walcott 1996; Witten et al. 2010), and the actual hierarchy of cues appears to depend strongly on the spatial scale. Generally , birds are not well adapted to conditions of zero visibility and except for some cave-dwelling oilbirds and swiftlets, which have evolved some rudimentary echolocation (Jordan Price et al. 2004), and owls, which position acoustic signals with great accuracy (Knudsen et al. 1979; Konishi 2003), the ability of birds to use sounds to locate objects does not rival that of the bats or dolphins. "
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    acta ethologica 03/2014; 17(1). DOI:10.1007/s10211-013-0155-3 · 1.00 Impact Factor
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    • "Medium spiny projection neurons seem to be devoid of nAChRs (Jones et al., 2001; Zhou et al., 2002) but fastspiking GABA interneurons (which comprise a tiny proportion of the total neuronal population) were shown to respond to the application of ACh or carbachol in a manner consistent with somatodendritic (possibly extrasynaptic) nAChRs (Koós and Tepper, 2002). In an elegant study, photoactivation of optogenetically engineered cholinergic interneurons of the nucleus accumbens resulted in an increased frequency of inhibitory currents in medium spiny neurons, and this response was sensitive to mecamylamine (Witten et al., 2010). The network connections mediating the increased firing rate are unclear, but it is plausible that GABAergic interneurons bearing nAChRs are involved, rather than a direct cholinergic action on medium spiny neurons. "
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    • "Auditory stimuli were generated using customized Matlab software interfaced with Tucker Davis Technologies hardware (RP2). Sounds were filtered with head-related transfer functions from a typical barn owl (Witten et al. 2010) and delivered binaurally through matched earphones (ED-1914; Knowles Electronics, Itasca, IL) coupled to damping assemblies (BF-1743) inserted into the ear canals ϳ5 mm from the eardrums. The amplitudes of the two earphones were equalized to within Ϯ 2 dB. "
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    ABSTRACT: Gamma-band (25-140 Hz) oscillations of the local field potential (LFP) are evoked by sensory stimuli in the mammalian forebrain and may be strongly modulated in amplitude when animals attend to these stimuli. The optic tectum (OT) is a midbrain structure known to contribute to multimodal sensory processing, gaze control, and attention. We found that presentation of spatially localized stimuli, either visual or auditory, evoked robust gamma oscillations with distinctive properties in the superficial (visual) layers and in the deep (multimodal) layers of the owl's OT. Across layers, gamma power was tuned sharply for stimulus location and represented space topographically. In the superficial layers, induced LFP power peaked strongly in the low-gamma band (25-90 Hz) and increased gradually with visual contrast across a wide range of contrasts. Spikes recorded in these layers included presumptive axonal (input) spikes that encoded stimulus properties nearly identically with gamma oscillations and were tightly phase locked with the oscillations, suggesting that they contribute to the LFP oscillations. In the deep layers, induced LFP power was distributed across the low and high (90-140 Hz) gamma-bands and tended to reach its maximum value at relatively low visual contrasts. In these layers, gamma power was more sharply tuned for stimulus location, on average, than were somatic spike rates, and somatic spikes synchronized with gamma oscillations. Such gamma synchronized discharges of deep-layer neurons could provide a high-resolution temporal code for signaling the location of salient sensory stimuli.
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