Localization and Identification of Concurrent Sounds in the Owl's Auditory Space Map

Abstract

In nature, sounds from multiple sources sum at the eardrums, generating complex cues for sound localization and identification. In this clutter, the auditory system must determine "what is where." We examined this process in the auditory space map of the barn owl's (Tyto alba) inferior colliculus using two spatially separated sources simultaneously emitting uncorrelated noise bursts, which were uniquely identified by different frequencies of sinusoidal amplitude modulation. Spatial response profiles of isolated neurons were constructed by testing the source-pair centered at various locations in virtual auditory space. The neurons responded whenever a source was placed within the receptive field, generating two clearly segregated foci of activity at appropriate loci. The spike trains were locked strongly to the amplitude modulation of the source within the receptive field, whereas the other source had minimal influence. Two sources amplitude modulated at the same rate were resolved successfully, suggesting that source separation is based on differences of fine structure. The spike rate and synchrony were stronger for whichever source had the stronger average binaural level. A computational model showed that neuronal activity was primarily proportional to the degree of matching between the momentary binaural cues and the preferred values of the neuron. The model showed that individual neurons respond to and synchronize with sources in their receptive field if there are frequencies having an average binaural-level advantage over a second source. Frequencies with interaural phase differences that are shared by both sources may also evoke activity, which may be synchronized with the amplitude modulations from either source.

Representation of Concurrent Stimuli by Population Activity in Visual Cortex

“…Effects of this kind have been observed in single neurons of regions as diverse as cortical area MT (Britten and Heuer, 1999; Heuer and Britten, 2002) and inferior colliculus (Keller and Takahashi, 2005). They may be due to normalization operating in the population responses in those regions or in earlier stages.…”

Spatial Hearing in Echoic Environments: The Role of the Envelope in Owls

“…When two sources concurrently emit sounds with overlapping amplitude spectra, the frequency-specific binaural cues assume values that are the average of each individual source’s cues weighted by their amplitudes. Thus, if one of the two sources momentarily achieves a higher amplitude than the other, the binaural cues approximate the values of the higher-amplitude source for that moment (Blauert, 1997; Keller and Takahashi, 2005; Snow, 1954; Takahashi and Keller, 1994). A space map neuron is therefore likely to fire when the amplitude modulation at a given instant favors the target, which is in its SRF, over the masker.…”

“…Although the two sounds’ carriers were identical, the 3-ms delay causes segments of the waveform in the leading source to align with segments in the lagging source that were 3 ms earlier and were therefore statistically uncorrelated in their fine-structure. Earlier studies have shown that the owl’s auditory system represents two, concomitant, uncorrelated noises as separate foci of activity on its auditory space map and that a delay of about 0.1 ms (100 μs) is sufficient to cause such decorrelation (Keller and Takahashi, 1996a, 2005). Thus, the decorrelated fine-structure allows two separate foci to form, while the envelope determines their relative strengths.…”

“…With shallower modulations, neither source had an amplitude advantage over the other (ΔE ≈ 0), and the rises in amplitudes were slow ( dĒ/dt ≈ 0). Thus, for delays tested here and a short integration time window (Joris et al, 2006; Siveke et al, 2008; Wagner, 1991, 1992), the lead/lag pair becomes equivalent to two, simultaneous, uncorrelated noises, to each of which, the space map neurons respond weakly (Keller and Takahashi, 2005). …”

New perspectives on the owl's map of auditory space

“…Although ITD and ILD alone are sufficient to drive orienting behavior [8,21], owls as well as mammals can also rely on spectral cues for locating and identifying sound sources in space [22,23]. It has been shown that midbrain space-specific neurons display frequency dependent tuning to ITD and ILD [24,25].…”