Abstract
Interaural time differences (ITDs) are an important cue for the localization of sounds in azimuthal space. Both birds and mammals have specialized, tonotopically organized nuclei in the brain stem for the processing of ITD: medial superior olive in mammals and nucleus laminaris (NL) in birds. The specific way in which ITDs are derived was long assumed to conform to a delay-line model in which arrays of systematically arranged cells create a representation of auditory space with different cells responding maximally to specific ITDs. This model was supported by data from barn owl NL taken from regions above 3 kHz and from chicken above 1 kHz. However, data from mammals often do not show defining features of the Jeffress model such as a systematic topographic representation of best ITDs or the presence of axonal delay lines, and an alternative has been proposed in which neurons are not topographically arranged with respect to ITD and coding occurs through the assessment of the overall response of two large neuron populations, one in each hemisphere. Modeling studies have suggested that the presence of different coding systems could be related to the animal’s head size and frequency range rather than their phylogenetic group. Testing this hypothesis requires data from across the tonotopic range of both birds and mammals. The aim of this study was to obtain in vivo recordings from neurons in the low-frequency range (<1000 Hz) of chicken NL. Our data argues for the presence of a modified Jeffress system that uses the slopes of ITD-selective response functions instead of their peaks to topographically represent ITD at mid- to high frequencies. At low frequencies, below several 100 Hz, the data did not support any current model of ITD coding. This is different to what was previously shown in the barn owl and suggests that constraints in optimal ITD processing may be associated with the particular demands on sound localization determined by the animal’s ecological niche in the same way as other perceptual systems such as field of best vision.
Highlights
Interaural time differences (ITDs) are the small differences in the arrival of a sound at the two ears of an animal
We tested each of the examined parameters for differences between data taken for different breeds; Kruskal– Wallis test, p = 0.616 for best ITD, p = 0.405 for best interaural phase difference (IPD), p = 0.068 for characteristic delay (CD), and p = 0.303 for characteristic phase (CP)
We report a total of 124 recordings from chicken nucleus laminaris (NL), of which 28 were extracellular single unit recordings, 31 were multiunit spike recordings (Figure 2B) and 65 were neurophonic recordings (Figure 2C)
Summary
Interaural time differences (ITDs) are the small differences in the arrival of a sound at the two ears of an animal. ITD computing is first carried out in specific, tonotopically organized areas of the brainstem nucleus laminaris (NL) in birds and the medial superior olive (MSO) in mammals Neurons in these nuclei act as coincidence detectors, firing maximally when the phase of the inputs from both ears is the same (Goldberg and Brown, 1969; Carr and Konishi, 1990; Yin and Chan, 1990). Data from birds and crocodilians (archosaurs) support a system of axonal time delay lines, as first suggested by Jeffress (1948) that creates a topographic array of NL neurons, each responding maximally to sounds from a specific ITD Together, these form a map or place code of azimuthal space (reviewed in Ashida and Carr, 2011)
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