Sound localization: Jeffress and beyond

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Many animals use the interaural time differences (ITDs) to locate the source of low frequency sounds. The place coding theory proposed by Jeffress has long been a dominant model to account for the neural mechanisms of ITD detection. Recent research, however, suggests a wider range of strategies for ITD coding in the binaural auditory brainstem. We discuss how ITD is coded in avian, mammalian, and reptilian nervous systems, and review underlying synaptic and cellular properties that enable precise temporal computation. The latest advances in recording and analysis techniques provide powerful tools for both overcoming and utilizing the large field potentials in these nuclei.

Highlights

► New theories have emerged to describe neural coding of interaural time differences. ► Birds, mammals, and lizards use various coding strategies for locating sound. ► Nevertheless, the underlying synaptic and cellular properties are very similar. ► Advanced techniques enable overcoming and utilizing the large field potentials.

Section snippets

The Jeffress model, its variants and alternatives

How can an animal tell the direction a sound is coming from? In 1948, American psychologist Lloyd Jeffress published a germinal paper [1], in which he proposed that the time difference of low frequency sounds arriving at the two ears (interaural time difference, ITD) can be represented as a ‘place’ in an array of nerve cells. The place theory (hereafter also referred to as the Jeffress model) depends on three fundamental assumptions: (1) orderly arrangement in conduction times of ascending

Synaptic and cellular properties

In spite of their different ITD coding strategies, the avian and mammalian auditory brainstems have a great deal in common, including very similar synaptic [16] and cellular [17] mechanisms. This convergence in functional organization reveals basic design features in species that possess unique evolutionary histories but use similar algorithms to solve basic computational problems [18].

Recordings from MSO and NL in vivo

Sound-induced extracellular field potentials are commonly found in many auditory stations in various animals. This field potential is termed the ‘neurophonic’ since it replicates the waveform of the stimulus tone (see [57] for a review). In NL and MSO, the amplitude of the neurophonic often lies in the millivolt range, hiding small somatic spikes (discussed above) in the background. This makes extracellular single unit recording in these nuclei particularly difficult [58]. There are two types

Concluding remarks

Beginning with the Jeffress model, recent studies of sound localization have revealed the presence of multiple ITD coding strategies in birds and mammals. Notwithstanding these differences, all ITD coding depends on the accurate representation of temporal information, which is mediated by similar or identical synaptic and cellular properties. Furthermore, the different ITD coding strategies are not always mutually exclusive; for example, owls may use slopes of the ITD tuning curves in the

Conflict of interest statement

The authors declare that they have no conflict of interest.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

This work was supported by NIH DC00436 to CEC, NIH P30 DC04664 to the University of Maryland Center for the Evolutionary Biology of Hearing. The authors thank Katrina MacLeod for comments on the manuscript, Yukiyo Nakayama-Ashida for comments on the figure.

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