Review
Detecting interaural time differences and remodeling their representation

https://doi.org/10.1016/j.tins.2014.03.002Get rights and content

Highlights

  • Across species, interaural time differences are detected by different mechanisms.

  • The detection stage serves as a database for higher auditory areas.

  • ITD representation is remodeled along the ascending auditory pathway.

  • Across species, ITD is represented in few broadly tuned channels in the forebrain.

  • Forebrain ITD representations likely subserve spatial unmasking.

Interaural time differences (ITDs) represent an important cue in sound localization and auditory scene analysis. To assess this cue the auditory system internally delays binaural inputs to compensate for the outer delay, before neurons in the brainstem detect the coincident arrival of the inputs from the two ears. Different origins of internal delays have been controversially discussed and have given rise to conflicting interpretations of the ITD representation ensuing from coincidence detection. Yet, recent findings indicate that ITD representations undergo substantial transformations or remodeling after the detection step. Here we treat the detection step separately from remodeling, and explain why a similar representation of ITD across species may exist in the forebrain despite differences in detection and representation in the midbrain.

Introduction

In everyday life humans and animals effortlessly localize sound sources with their ears. They can do this much more precisely with two ears than with one [1]. This is strongly experienced by people having unilateral hearing loss [2]. It is currently a challenge to develop binaural cochlear implants that improve the user's sound-localization capabilities and sound perception 3, 4, 5. To do so, it is necessary to understand the mechanisms underlying the representation of sound-localization information in healthy brains. In this review we discuss advances in one sound-localization cue, the ITD (see Glossary), which has received increased interest recently due to new but still controversial findings of its representation in the brain.

ITDs arise from path-length differences between the sound source and the two ears, and correlate with azimuth, the angle between a sound source and the medial plane. The physiological ITD range (gerbil, ±120 μs [6]; barn owl, ±250 μs [7]; human, ±600 μs [1]) depends on the head size of the animal and the morphology of aural appendages such as the ear flaps in humans or the ruff of the barn owl. After the signal reaches the ear the temporal relationships at the ear drum are conserved throughout monaural processing and lead to a step of binaural interaction, in which tuning to and a representation of ITD emerges in the brainstem. Further processing steps then follow along the auditory processing pathways.

Current research tries to identify the mechanisms underlying the binaural interaction, to characterize subsequent processing, and to find out how the representation of ITD may interact with higher brain functions and drive motor networks.

An influential theory detailing how ITD might be computed in the brain was proposed by Jeffress in 1948 [8] (Box 1). His model assumes three basic elements underlying the representation of ITD: neurons acting as coincidence detectors, time delays, and an arrayed arrangement of these cells resulting in a place map of ITD. Since then vast progress has been made from the molecular to the systems level. Although several reviews on this topic are available 9, 10, we want to stress here that the processing level dealt with by Jeffress is only the first step in the representation of ITD. We shall refer to this first processing step as the detection of ITD and we review recent advances regarding the diversity of proposed mechanisms as well as their strengths and weaknesses in the next section. The sensitivity to ITD extracted at the detection step does not drive motor output directly, presumably because it lacks a suitable format. Instead the signal is transformed through further processing which takes place in two main parallel pathways within the ascending auditory system. We shall refer to these further processing steps as remodeling because they may change the code underlying the representation of ITD, as we shall show in the second section of this review.

By separating the detection step from the remodeling we show that neurons on the first step reveal properties of the detection mechanism in their responses, but that this signature may be lost throughout remodeling and instead other qualities emerge that potentially reflect adaptations to behaviors that make use of ITD information.

Section snippets

Diversity in ITD detection

Neurons detecting ITDs by a coincidence mechanism have been found in a wide range of vertebrates, including birds, reptiles, and mammals (9, 10 for review). The site of binaural interaction is the nucleus laminaris (NL) in birds, and the medial superior olive (MSO) plus – for ITDs in the signal envelope – the lateral superior olive (LSO) in mammals, all situated in the hindbrain. While it is largely accepted that the cells in these nuclei function as coincidence detectors (Box 2), the main

Remodeling the representation of ITD

Transformations of the ITD representation occur after the detection stage (Figure 2). We shall refer to these transformations as ‘remodeling’ in the following. If frequency and ITD are regarded and other influences are disregarded, in principle, four scenarios for remodeling are possible as summarized in Box 3. The results of remodeling may simply be an improvement of the signal-to-noise ratio or they may lead to a transformation of the code at both the single-neuron and population levels.

Functional roles of ITD

The use of ITD in orienting responses is obvious, but ITDs have more functions in driving behavior. These different functions may necessitate different formats of representations. This could explain why in the midbrain of barn owls ITDs form a map of auditory space that is the basis for orienting responses 71, 72, 73, 74, whereas in the forebrain such a space map is missing [75].

The functions of the forebrain in auditory streaming are manifold and include localization [76], attention control 77

Concluding remarks

Humans and other species use ITD primarily for sound localization, but this cue has more functions in, for instance, spatial unmasking. This is why binaural cochlear implants that are able to utilize ITD information will greatly improve not only sound-localization but also auditory scene analysis capabilities of their wearer. This step has not yet been reached, but the findings on ITD detection reported here may provide a basis for the correct targeting of the binaural cells with the signals

Acknowledgments

We thank the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG) for funding our research on the auditory system (VO 1980/1-1, Wa606/21-1), R. Felix for carefully reading and commenting on the manuscript, and an anonymous reviewer for his thorough and constructive criticism.

Glossary

Characteristic delay (CD) and characteristic phase (CP)
parameters that describe the ITD tuning across different frequencies in a neuron. The CD reveals the frequency-independent component of tuning to ITD whereas the CP describes the frequency-dependent component. CD and CP represent slope and offset, respectively, of the linear relation between preferred interaural phase difference (IPD) and stimulus frequency, and thus are either both defined or both undefined, if the relation is nonlinear.

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