The ability to determine the location of a sound source is fundamental to hearing. However, auditory space is not represented in any systematic manner on the basilar membrane of the cochlea, the sensory surface of the receptor organ for hearing. Understanding the means by which sensitivity to spatial cues is computed in central neurons can therefore contribute to our understanding of the basic nature of complex neural representations. We review recent evidence concerning the nature of the neural representation of auditory space in the mammalian brain and elaborate on recent advances in the understanding of mammalian subcortical processing of auditory spatial cues that challenge the "textbook" version of sound localization, in particular brain mechanisms contributing to binaural hearing.

Mechanisms of Sound Localization in Mammals

The planum temporale as a computational hub

Because the inner ear is not organized spatially, sound localization relies on the neural processing of implicit acoustic cues. To determine a sound's position, the brain must learn and calibrate these cues, using accurate spatial feedback from other sensorimotor systems. Experimental evidence for such a system has been demonstrated in barn owls, but not in humans. Here, we demonstrate the existence of ongoing spatial calibration in the adult human auditory system. The spectral elevation cues of human subjects were disrupted by modifying their outer ears (pinnae) with molds. Although localization of sound elevation was dramatically degraded immediately after the modification, accurate performance was steadily reacquired. Interestingly, learning the new spectral cues did not interfere with the neural representation of the original cues, as subjects could localize sounds with both normal and modified pinnae.

/pdf/relearning-sound-localization-with-new-ears-5bsjfcqcb8.pdf

Relearning sound localization with new ears.

In Drosophila and mice, olfactory receptor neurons (ORNs) expressing the same receptors have convergent axonal projections to specific glomerular targets in the antennal lobe/olfactory bulb, creating an odour map in this first olfactory structure of the central nervous system1,2,3. Projection neurons of the Drosophila antennal lobe send dendrites into glomeruli and axons to higher brain centres4, thereby transferring this odour map further into the brain. Here we use the MARCM method5 to perform a systematic clonal analysis of projection neurons, allowing us to correlate lineage and birth time of projection neurons with their glomerular choice. We demonstrate that projection neurons are prespecified by lineage and birth order to form synapses with specific incoming ORN axons, and therefore to carry specific olfactory information. This prespecification could be used to hardwire the fly's olfactory system, enabling stereotyped behavioural responses to odorants. Developmental studies lead us to hypothesize that recognition molecules ensure reciprocally specific connections of ORNs and projection neurons. These studies also imply a previously unanticipated role for precise dendritic targeting by postsynaptic neurons in determining connection specificity.

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Target neuron prespecification in the olfactory map of Drosophila.

Rapid reaching to a target is generally accurate but also contains random and systematic error. Random errors result from noise in visual measurement, motor planning, and reach execution. Systematic error results from systematic changes in the mapping between the visual estimate of target location and the motor command necessary to reach the target (e.g., new spectacles, muscular fatigue). Humans maintain accurate reaching by recalibrating the visuomotor system, but no widely accepted computational model of the process exists. Given certain boundary conditions, a statistically optimal solution is a Kalman filter. We compared human to Kalman filter behavior to determine how humans take into account the statistical properties of errors and the reliability with which those errors can be measured. For most conditions, human and Kalman filter behavior was similar: Increasing measurement uncertainty caused similar decreases in recalibration rate; directionally asymmetric uncertainty caused different rates in different directions; more variation in systematic error increased recalibration rate. However, behavior differed in one respect: Inserting random error by perturbing feedback position causes slower adaptation in Kalman filters but had no effect in humans. This difference may be due to how biological systems remain responsive to changes in environmental statistics. We discuss the implications of this work.

The statistical determinants of adaptation rate in human reaching.

This paper describes the effect of spectro-temporal factors on human sound localization performance in two dimensions (2D). Subjects responded with saccadic eye movements to acoustic stimuli presented in the frontal hemisphere. Both the horizontal (azimuth) and vertical (elevation) stimulus location were varied randomly. Three types of stimuli were used, having different spectro-temporal patterns, but identically shaped broadband averaged power spectra: noise bursts, frequency-modulated tones, and trains of short noise bursts. In all subjects, the elevation components of the saccadic responses varied systematically with the different temporal parameters, whereas the azimuth response components remained equally accurate for all stimulus conditions. The data show that the auditory system does not calculate a final elevation estimate from a long-term (order 100 ms) integration of sensory input. Instead, the results suggest that the auditory system may apply a “multiple-look” strategy in which the final estimate is calculated from consecutive short-term (order few ms) estimates. These findings are incorporated in a conceptual model that accounts for the data and proposes a scheme for the temporal processing of spectral sensory information into a dynamic estimate of sound elevation.

/pdf/spectro-temporal-factors-in-two-dimensional-human-sound-4cn9wl1u1h.pdf

Spectro-temporal factors in two-dimensional human sound localization

Human sound localization relies on binaural difference cues for sound-source azimuth and pinna-related spectral shape cues for sound elevation. Although the interaural timing and level difference cues are weighted to produce a percept of sound azimuth, much less is known about binaural mechanisms underlying elevation perception. This problem is particularly interesting for the frontal hemifield, where binaural inputs are of comparable strength. In this paper, localization experiments are described in which hearing for each ear was either normal, or spectrally disrupted by a mold fitted to the external ear. Head-fixed saccadic eye movements were used as a rapid and accurate indicator of perceived sound direction in azimuth and elevation. In the control condition (both ears free) azimuth and elevation components of saccadic responses were well described by a linear regression line for the entire measured range. For unilateral mold conditions, the azimuth response components did not differ from controls. The influence of the mold on elevation responses was largest on the ipsilateral side, and declined systematically with azimuth towards the side of the free ear. Near the midsagittal plane the elevation responses were clearly affected by the mold, suggesting a systematic binaural interaction in the neural computation of perceived elevation that straddles the midline. A quantitative comparison of responses from the unilateral mold, the bilateral mold and control condition provided evidence that the fusion process can be described by binaural weighted averaging. Two different conceptual schemes are discussed that could underlie the observed responses.

/pdf/binaural-weighting-of-pinna-cues-in-human-sound-localization-3alitgczmu.pdf

Binaural weighting of pinna cues in human sound localization.

The directionally sensitive acoustics of the pinnae enable humans to perceive the up-down and front-back direction of sound This mechanism complements another, independent mechanism that derives sound-source azimuth from interaural difference cues The pinnae effectively add direction-dependent spectral notches and peaks to the incoming sound, and it has been shown that such features are used to code sound direction in the median plane However, it is still unclear which of the pinna-induced features play a role in sound localization The present study presents a method for the reconstruction of the spatially relevant features in the spectral domain Broadband sounds with random spectral shapes were presented in rapid succession as subjects made saccadic eye movements toward the perceived stimulus locations The analysis, which is based on Bayesian statistics, indicates that specific spectral features could be associated with perceived spatial locations Spectral features that were determined by this psychophysical method resemble the main characteristics of the pinna transfer functions obtained from acoustic measurements in the ear canal Despite current experimental limitations, the approach may prove useful in the study of perceptually relevant spectral cues underlying human sound localization

Bayesian reconstruction of sound localization cues from responses to random spectra.

http://www.mbfys.ru.nl/~johnvo/papers/swappedhearing.pdf

Paul M. Hofman

Papers

Relearning sound localization with new ears.

Spectro-temporal factors in two-dimensional human sound localization

Binaural weighting of pinna cues in human sound localization.

Bayesian reconstruction of sound localization cues from responses to random spectra.

A method to induce swapped binaural hearing