Review
The shape of ears to come: dynamic coding of auditory space

https://doi.org/10.1016/S1364-6613(00)01660-0Get rights and content

Abstract

In order to pinpoint the location of a sound source, we make use of a variety of spatial cues that arise from the direction-dependent manner in which sounds interact with the head, torso and external ears. Accurate sound localization relies on the neural discrimination of tiny differences in the values of these cues and requires that the brain circuits involved be calibrated to the cues experienced by each individual. There is growing evidence that the capacity for recalibrating auditory localization continues well into adult life. Many details of how the brain represents auditory space and of how those representations are shaped by learning and experience remain elusive. However, it is becoming increasingly clear that the task of processing auditory spatial information is distributed over different regions of the brain, some working hierarchically, others independently and in parallel, and each apparently using different strategies for encoding sound source location.

Section snippets

Extraction of auditory localization cues in the brainstem

The neural processing of different auditory localization cues begins in largely separate pathways in the brainstem 4. Auditory nerve fibres leaving the cochlea terminate on neurones in different subdivisions of the cochlear nucleus. Cells in the ventral subdivisions project, either directly or indirectly, to the superior olivary complex (SOC) on both sides of the brainstem. The SOC is therefore the principal site of binaural convergence, and it is at this level that neuronal sensitivity to

Mapping auditory space in the midbrain

Free-field studies have shown that a map of auditory space exists within the deeper layers of the SC (Refs 10, 11, 12). This is defined by an orderly relationship between the preferred sound directions of auditory neurones and their location within the nucleus (Fig. 1). In contrast to most other relay stations between the cochlea and the cortex, the SC is not ‘tonotopically’ organized. Instead, spatial information is combined across different frequency-specific channels in the brainstem to

Alternative coding strategies in the cortex

Recent studies of the neural processing of auditory space have focused increasingly on the cortex. It has been known for a long time that temporal lobe damage can lead to impaired sound localization 17, 18. But lesion studies are not always easy to interpret, because it can be unclear whether an observed deficit is attributable to a sensory or perceptual loss, or an inability to generate or perform the correct response. Nevertheless, it has been concluded that, after large bilateral lesions of

Auditory localization is individually calibrated

The size and shape of the head and external ears, and therefore the values of the auditory localization cues corresponding to particular sound directions, can vary substantially between individuals 35, 36, 37. These cue values also undergo changes within a subject as the head and ears grow (Fig. 3). Accurate localization therefore requires that the neural code for auditory space be calibrated to these individual characteristics. Evidence for this has been provided in human psychophysical

Experience shapes the developing representation of auditory space

Most of the neurophysiological evidence for experience-driven adjustments in sound localization has come from developmental studies of the auditory space map in the SC. Experiments in which animals have been reared with modified auditory or visual inputs have revealed substantial plasticity in this representation 43, 44.

The potential for the sound localization pathway to be shaped by experience of the acoustic localization cues provided by the listener's own ears is illustrated by the

Plasticity of sound localization is not restricted to development

There is considerable evidence that neural circuits, and the behaviours to which they contribute, are particularly dependent on sensory experience during a ‘critical period’ of early life. The plasticity of the auditory space map in the SC is no exception to this, as the spatial tuning of these neurones is more susceptible to altered sensory inputs during infancy than later in life 43, 44. This makes good sense, as developmental plasticity is clearly necessary in order to adjust neuronal

Concluding remarks

The neural computations involved in determining the location of a sound source are established in the brainstem, but the manner in which this information is encoded changes at higher levels of the auditory system. The SC contains a topographic representation of auditory space, which contributes to the multisensory guidance of orienting behaviour. The steps leading to the formation of this neural map and its alignment with other sensory representations have provided a valuable and accessible

Questions for future research

  • How are the various schemes that have been proposed for coding space in the auditory cortex affected by the presence of multiple sound sources, or under conditions in which other features of the sound source vary? Are these coding schemes emergent properties of the cortex or do they originate in the subcortical nuclei that feed into A1?

  • Studies that emphasize the importance of temporal discharge patterns in auditory spatial coding have mostly been carried out on anaesthetized animals. What is

Acknowledgements

Our research is supported by the Wellcome Trust (Senior Research Fellowship to A.J.K.) and by Defeating Deafness (Dunhill Medical Trust Fellowship to J.W.H.S.). We are grateful to Tom Mrsic-Flogel and to Doris Kistler for their assistance with recording some of the data illustrated in this paper, and to David Moore, Tom Mrsic-Flogel and Carl Parsons for their comments on an earlier draft of the manuscript.

References (60)

  • B.J. May

    Role of the dorsal cochlear nucleus in the sound localization behavior of cats

    Hear. Res.

    (2000)
  • D.C. Fitzpatrick

    A neuronal population code for sound localization

    Nature

    (1997)
  • T.J. Park

    IID sensitivity differs between two principal centers in the interaural intensity difference pathway: the LSO and the IC

    J. Neurophysiol.

    (1998)
  • M.W. Spitzer et al.

    Transformation of binaural response properties in the ascending auditory pathway: influence of time-varying interaural phase disparity

    J. Neurophysiol.

    (1998)
  • A.J. King et al.

    Spatial response properties of acoustically responsive neurons in the superior colliculus of the ferret: a map of auditory space

    J. Neurophysiol.

    (1987)
  • E.I. Knudsen

    Auditory and visual maps of space in the optic tectum of the owl

    J. Neurosci.

    (1982)
  • J.C. Middlebrooks et al.

    A neural code for auditory space in the cat's superior colliculus

    J. Neurosci.

    (1984)
  • B.E. Stein et al.

    The Merging of the Senses

    (1993)
  • P.H. Hartline

    Effects of eye position on auditory localization and neural representation of space in superior colliculus of cats

    Exp. Brain Res.

    (1995)
  • M.F. Jay et al.

    Auditory receptive fields in primate superior colliculus shift with changes in eye position

    Nature

    (1984)
  • L.C. Populin et al.

    Sensitivity of auditory cells in the superior colliculus to eye position in the behaving cat

  • R.B. Masterton

    Role of the mammalian forebrain in hearing

  • H.E. Heffner et al.

    Effect of bilateral auditory cortex lesions on sound localization in Japanese macaques

    J Neurophysiol.

    (1990)
  • W.M. Jenkins et al.

    Role of cat primary auditory cortex for sound-localization behavior

    J. Neurophysiol.

    (1984)
  • J.P. Rauschecker et al.

    Mechanisms and streams for processing of ‘what’ and ‘where’ in auditory cortex

    Proc. Natl. Acad. Sci. USA

    (2000)
  • G.H. Recanzone

    Correlation between the activity of single auditory cortical neurons and sound-localization behavior in the macaque monkey

    J. Neurophysiol.

    (2000)
  • K.O. Bushara

    Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans

    Nat. Neurosci.

    (1999)
  • T.D. Griffiths

    Human brain areas involved in the analysis of auditory movement

    Hum. Brain Mapp.

    (2000)
  • J.F. Brugge

    The structure of spatial receptive fields of neurons in primary auditory cortex of the cat

    J. Neurosci.

    (1996)
  • T.J. Imig

    Single-unit selectivity to azimuthal direction and sound pressure level of noise bursts in cat high-frequency primary auditory cortex

    J. Neurophysiol.

    (1990)
  • Cited by (85)

    • 2.36 - Coding of Spatial Information

      2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition
    • Frequency-specific attentional modulation in human primary auditory cortex and midbrain

      2018, NeuroImage
      Citation Excerpt :

      Human FMRI studies of interaural attention (Rinne et al., 2008) and perceptual switches in auditory streaming (Schadwinkel and Gutschalk, 2011) found similar top-down attentional modulation in the absence of physical stimulus variations in human IC, but based on listeners' perceived location of the auditory targets. Given the prominent role of IC in spatial processing (King et al., 2001), these spatial cues have been suggested to be particularly effective in producing attentional modulation in human IC (Rinne et al., 2008). Our study suggests that sound processing in human IC may also be modulated by endogenous attention to spectral cues alone.

    • A selective impairment of perception of sound motion direction in peripheral space: A case study

      2016, Neuropsychologia
      Citation Excerpt :

      This suggests that the difference in the acoustic feature to be analyzed (spectral vs. binaural) as well as the perceptual attribute that needs to be judged (location vs. motion speed vs. motion direction) have to be considered together when characterizing the deficit we observed in MC. Spectral and binaural cues are processed along separate pathways in the auditory system (e.g. King et al., 2001). Our results suggest that there might also be separate processing of spectral vs. binaural cues for different aspects of auditory spatial perception.

    View all citing articles on Scopus
    View full text