Trends in Neurosciences
ReviewDetecting interaural time differences and remodeling their representation
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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2019, Hearing ResearchCitation Excerpt :For this, auditory information from both inner ears needs to be compared. Because major cues used for localization are not contained in the monaural signal, they must be computed by the nervous system (Grothe et al., 2010; Vonderschen and Wagner, 2014). A number of these computational steps, which take place in binaural neurons in the superior olivary complex (Goldberg and Brown, 1969; Pecka et al., 2008; Yin and Chan, 1990), rely on a faithful representation of the temporal structure of the sound (Oertel, 1999).
Binaural unmasking of the accuracy of envelope-signal representation in rat auditory cortex but not auditory midbrain
2019, Hearing ResearchCitation Excerpt :Differences in temporal frequency encoding between IC and AC may also influence neuronal sensitivity to ITDs (Belliveau et al., 2014; Lohuis and Fuzessery, 2000; Vonderschen and Wagner, 2014). For example, previous studies have demonstrated that the ITD sensitivity in pallid bats markedly increases from the midbrain to the cortex (Lohuis and Fuzessery, 2000), and that the ITD representation undergoes substantial transformations (Vonderschen and Wagner, 2014). Thus, the differences between the IC and the AC in binaural unmasking effects on the accuracy of neural representations of sound signals may reveal specific substrates underlying that effect.