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  • Review Article
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New roles for synaptic inhibition in sound localization

Nature Reviews Neuroscience volume 4, pages 540–550 (2003)Cite this article

Key Points

  • Interaural time differences (ITDs) are the main cue for localizing low-frequency sounds. As they are only in the range of microseconds, ITD detection requires the most elaborate mechanism for temporal processing in the mammalian or avian brain.

  • The textbook view of how ITD processing is achieved has been dominated by the seminal model put forward by Jeffress in 1948. This model incorporates excitatory projections from both ears that faithfully time-lock to the temporal structure of sounds and converge onto binaural coincidence detector neurons. These fire maximally when the two inputs arrive simultaneously. The model also assumes that a systematic arrangement of the length of the input fibres (delay lines), can produce different conductance delays that tune different coincidence detector neurons to different favoured ITDs. Such a system could then create a map of best ITDs, and hence of azimuthal space.

  • ITD-sensitive coincidence detector neurons have been found in the mammalian medial superior olive (MSO) and in its avian analogue, the nucleus laminaris. In the bird ITD-processing circuits, delay lines have been described structurally and functionally, and there is good evidence for a topographic representation of ITDs (and, hence, of azimuthal space) at least in the barn owl auditory system. By contrast, the existence of delay lines in mammals has been controversial, and convincing evidence for topographic maps of ITDs is lacking. Recent evidence indicates that, in mammals, the representation of azimuthal space calculated from ITDs might be organized in a fundamentally different way than proposed by Jeffress.

  • Our view of the representation of ITDs in mammals, and also of the mechanism of ITD processing itself, is undergoing marked changes. In birds and mammals, profound inhibitory inputs have to be added to our picture of ITD processing. These inhibitory inputs have entirely different functions in birds and mammals. Whereas in birds tonic depolarizing GABA (γ-aminobutyric acid)-mediated inhibition accounts for differential gain control and a general improvement of the coincidence detection mechanism, temporally precise inhibition onto ITD-sensitive neurons in the mammalian MSO actively contributes to the ITD tuning itself.

  • The ITD-processing circuits in birds and mammals are an excellent example of how evolution of the vertebrate nervous system can produce very different functional solutions for the same computational problem.

Abstract

The arrival times of a sound at the two ears are only microseconds apart, but both birds and mammals can use these interaural time differences to localize low-frequency sounds. Traditionally, it was thought that the underlying mechanism involved only coincidence detection of excitatory inputs from the two ears. However, recent findings have uncovered profound roles for synaptic inhibition in the processing of interaural time differences. In mammals, exquisitely timed hyperpolarizing inhibition adjusts the temporal sensitivity of coincidence detector neurons to the physiologically relevant range of interaural time differences. Inhibition onto bird coincidence detectors, by contrast, is depolarizing and devoid of temporal information, providing a mechanism for gain control.

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Figure 1: The evolution of tympanic ears.
Figure 2: The interaural time difference (ITD).
Figure 3: Different strategies for encoding interaural time differences (ITDs).
Figure 4: The interaural time difference (ITD)-encoding systems in mammals and birds.
Figure 5: The role of inhibition in the medial superior olive (MSO).
Figure 6: Inhibitory inputs to medial superior olive (MSO) cells become refined to cell somata.

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Authors and Affiliations

  1. Max-Planck-Institute of Neurobiology, Auditory Processing Group, Am Klopferspitz 18a, Martinsried, D-82152, Germany

    Benedikt Grothe

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FURTHER INFORMATION

Encyclopedia of Life Sciences

prey detection by bats and owls

Benedikt Grothe's Lab

Glossary

INTERAURAL TIME DIFFERENCE

(ITD). The difference in the arrival time of a sound at the two ears. Depending on the position of the sound source and the individual inter-ear distance, ITDs can be up to about 120 μs in the Mongolian gerbil, and up to about 650 μs in humans.

TIME-LOCKED

Action potentials of many auditory neurons are locked to specific events of acoustic stimuli, such as onsets, offsets, prominent fluctuations in frequency or amplitude, or even a specific phase-angle of sinusoidal low-frequency sounds.

PHASE-LOCKED

The most extreme case of time-locking in auditory neurons. Many low-frequency neurons (in mammals up to a few kHz, in barn owls up to 8 kHz) synchronize their discharge to a specific phase-angle of tones.

COINCIDENCE DETECTION

The activation of neurons not by single inputs, but only by the simultaneous activity of several inputs. Coincidence detector neurons can be found throughout the nervous system. The most extreme case of coincidence detection is found in the binaural auditory system where the time windows for coincidence detection are in the range of microseconds.

AZIMUTHAL SPACE

The definition of auditory space independent of the elevation of a sound source. The task of localizing a sound in azimuthal space is often referred to as 'lateralization'.

MEDIAL NUCLEUS OF THE TRAPEZOID BODY

(MNTB). Its neurons receive their inputs through the largest and temporally most secure synapse, the calyx of Held. MNTB neurons contain the highest concentration of the inhibitory transmitter glycine in the mammalian brain and project to several brainstem structures, among them the medial superior olive. No structural or functional analogue of MNTB is known in birds.

DEPOLARIZING INHIBITION

Inhibition is thought to function by hyperpolarization of the membrane potential of the target cell owing to the opening of Cl− channels. However, in some neurons, release of inhibitory transmitters can cause depolarization, which in turn activates other channels that prevent the cell from reaching spike threshold. Whether the opening of Cl− channels hyperpolarizes or depolarizes a cell depends on its Cl− reversal potential.

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Grothe, B. New roles for synaptic inhibition in sound localization. Nat Rev Neurosci 4, 540–550 (2003). https://doi.org/10.1038/nrn1136

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