Creating a sense of auditory space

Abstract

Determining the location of a sound source requires the use of binaural hearing--information about a sound at the two ears converges onto neurones in the auditory brainstem to create a binaural representation. The main binaural cue used by many mammals to locate a sound source is the interaural time difference, or ITD. For over 50 years a single model has dominated thinking on how ITDs are processed. The Jeffress model consists of an array of coincidence detectors--binaural neurones that respond maximally to simultaneous input from each ear--innervated by a series of delay lines--axons of varying length from the two ears. The purpose of this arrangement is to create a topographic map of ITD, and hence spatial position in the horizontal plane, from the relative timing of a sound at the two ears. This model appears to be realized in the brain of the barn owl, an auditory specialist, and has been assumed to hold for mammals also. Recent investigations, however, indicate that both the means by which neural tuning for preferred ITD, and the coding strategy used by mammals to determine the location of a sound source, may be very different to barn owls and to the model proposed by Jeffress.

Figure 1. The Jeffress model of binaural coincidence detection

The model consists of an array of coincidence detectors – neurones that respond maximally when inputs arrive from the two ears simultaneously – innervated from each ear by a series of delay lines – axons of variable path length. The purpose of this arrangement is to create a map of auditory space from information about the relative time of arrival of a sound at the two ears.

Figure 2. Phase-locking and neural sensitivity to interaural time differences

A, illustration of the concept of phase-locking. In response to low-frequency (< 4 kHz) sounds, auditory nerve fibres preferentially fire at the same stimulus phase. Such phase-locking is a requirement of neural sensitivity to interaural time differences (ITDs). B, response of a neurone in the inferior colliculus of the guinea pig to interaurally delayed pure tones of various frequencies. Note the cyclic nature of the response for each frequency, and the alignment at just one ITD of a peak response across all the functions.

Figure 3. ITD tuning sharpness and sound-frequency tuning

A, hypothetical frequency tuning curves of a mammalian (red) and a barn owl (blue) auditory neurone. The sound frequency range over which ITDs are processed is an order of magnitude higher in barn owls as compared to mammals. B, hypothetical ITD functions for mammalian (red) and barn owl (blue) binaural neurones. The high frequency range over which barn owls process ITDs as compared to mammals renders their ITD functions much more sharply tuned relative to the physiological range of ITDs they can experience (denoted by line with arrowheads on abscissa) as compared to mammals with a similarly sized head.

Figure 4. Preferred tuning for ITDs is dependent on neural CF

A, responses of 6 typical inferior colliculus neurones to interaurally delayed noise (the damped side peaks of the responses are hidden to aid visual inspection). The neurone with the lowest sound-frequency tuning shows the widest function which peaks at the longest ITD. Neurones with tuning to progressively higher sound frequencies show systematically narrow functions and peak responses that lie closer to zero ITD. The grey shaded area indicates the physiological range of ITDs (approx. ± 180 ms) in the guinea pig. B, location of peak responses for a population of neurones recorded in the inferior colliculus of the guinea pig. The positions of the peak responses of the 6 neurones in A are indicated by the appropriately coloured dots. The line indicates the ITD equivalent to 45 deg interaural phase difference. The grey shaded area indicates the physiological range.

Figure 5. Modelling binaural hearing

A, hemispheric channels model of spatial hearing. See text for further details. B: top, ideal distributions of tuning curves for coding ITDs (here plotted as interaural phase differences, IPDs) for 500 Hz tones in gerbil for left (red) and right (blue) subpopulations. Dotted lines show a measure of coding efficiency – Fisher information – which is maximal over the physiological range (shaded grey area); bottom, ideal distribution for coding IPDs of 5000 Hz tones in barn owl (sample only shown). Red lines show tuning curve (continuous line) and scaled Fisher information (dotted lines) for one neurone (modified from Fig. 2 in Harper & McAlpine, 2004).