Elsevier

Neuropsychologia

Volume 48, Issue 9, July 2010, Pages 2610-2619
Neuropsychologia

Processing of binaural spatial information in human auditory cortex: Neuromagnetic responses to interaural timing and level differences

https://doi.org/10.1016/j.neuropsychologia.2010.05.008Get rights and content

Abstract

This study was designed to test two hypotheses about binaural hearing: (1) that binaural cues are primarily processed in the hemisphere contralateral to the perceived location of a sound; and (2) that the two main binaural cues, interaural timing differences and interaural level differences, are processed in separate channels in the auditory cortex. Magnetoencephalography was used to measure brain responses to dichotic pitches – a perception of pitch created by segregating a narrow band of noise from a wider band of noise – derived from interaural timing or level disparities. Our results show a strong modulation of interhemispheric M100 amplitudes by ITD cues. When these cues simulated source presentation unilaterally from the right hemispace, M100 amplitude changed from a predominant right hemisphere pattern to a bilateral pattern. In contrast, ILD cues lacked any capacity to alter the right hemispheric distribution. These data indicate that intrinsic hemispheric biases are large in comparison to any contralaterality biases in the auditory system. Importantly, both types of binaural cue elicited a circa 200 ms latency object-related negativity component, believed to reflect automatic cortical processes involved in distinguishing concurrent auditory objects. These results support the conclusion that ITDs and ILDs are processed by distinct neuronal populations to relatively late stages of cortical processing indexed by the M100. However information common to the two cues seems to be extracted for use in a subsequent stage of auditory scene segregation indexed by the object related negativity. This may place a new bound on the extent to which sound location cues are processed in separate channels of the auditory cortex.

Section snippets

Subjects

Twelve right-handed subjects (7 male, mean age = 29.3) with no reported history of auditory or neurological illness took part. The project was approved by the Macquarie University Human Participants Ethics Committee.

Experimental design

The basic acoustic stimulus was a 500 ms broadband noise. When this stimulus is duplicated and presented identically to both ears, the percept is of a noise located in the centre of the head. When an interaural disparity (timing or level) is introduced, the noise is perceived to be

Behavioural data

The average values of d′ across all subjects were: right-leading ITD (d = 2.2, SE = 0.3), left-leading ITD (d = 2.4, SE = 0.4), right-leading ILD (d = 3.0, SE = 0.4), and left-leading ILD (d = 3.3, SE = 0.4). ANOVA (location cue type by leading ear) confirmed an effect of location cue type (F(1,11) = 9.62, p = .01). Despite the matching procedure, the ILD stimuli (d = 3.1, SE = 0.3) were still more detectable than the ITD stimuli (d = 2.3, SE = 0.2). All other effects were not significant.

MEG data

The acoustic stimuli

Discussion

Our study examined the processing of binaural spatial information in the human auditory cortex. We used a psychophysical paradigm, termed “dichotic pitch,” in which listeners are able to use azimuthal location cues to separate a complex sound into two concurrent percepts. This paradigm had two key features. First, it allowed us to produce binaural stimuli containing either a single lateralized sound or two lateralized sounds located in opposite hemispaces. Second, we were able to generate

Conclusions

Our results show a strong modulation of interhemispheric activity by ITD cues, but only when these cues are presented unilaterally from the right hemispace. Our data support the interpretation of a relatively strong right hemisphere bias for spatial information in conjunction pitted against a relatively weaker left hemisphere preference for timing information. The hemispheric biases are large in comparison to the modest contralateral bias exhibited at the population level in primate auditory

Acknowledgements

This work was supported by Australian Research Council Linkage Infrastructure Equipment and Facilities Grant LEO668421. The authors gratefully acknowledge the collaboration of Kanazawa Institute of Technology and Yokogawa Electric Corporation in establishing the KIT-Macquarie MEG laboratory. We thank Melanie Reid and Graciela Tesan for assistance with data collection. The authors thank two anonymous reviewers whose comments greatly improved an earlier version of this manuscript.

References (50)

  • H. Wagner

    A comparison of neural computations underlying stereo vision and sound localization

    Journal of Physiology (Paris)

    (2004)
  • K. Yamada et al.

    Sound lateralization in patients with lesions including the auditory cortex: Comparison of interaural time difference, (ITD) discrimination and interaural intensity difference (IID) discrimination

    Hearing Research

    (1996)
  • U. Zimmer et al.

    Processing of auditory spatial cues in human cortex: An fMRI study

    Neuropsychologia

    (2006)
  • U. Zimmer et al.

    High binaural coherence determines successful sound localization and increased activity in posterior auditory areas

    Neuron

    (2005)
  • C. Alain et al.

    Bottom-up and top-down influences on auditory scene analysis: Evidence from event-related brain potentials

    Journal of Experimental Psychology: Human Perception and Performance

    (2001)
  • C. Alain et al.

    Age-related differences in neuromagnetic brain activity underlying concurrent sound perception

    Journal of Neuroscience

    (2007)
  • C. Alain et al.

    Neural activity associated with distinguishing concurrent auditory objects

    Journal of the Acoustical Society of America

    (2002)
  • A.S. Bregman

    Auditory scene analysis: The perceptual organization of sound

    (1990)
  • M. Brunetti et al.

    Human brain activation during passive listening to sounds from different locations: An fMRI and MEG study

    Human Brain Mapping

    (2005)
  • M. Chait et al.

    Neural response correlates of detection of monaurally and binaurally created pitches in humans

    Cerebral Cortex

    (2006)
  • M. Corbetta et al.

    Control of goal-directed and stimulus-driven attention in the brain

    Nature Reviews Neuroscience

    (2002)
  • R.F. Dougherty et al.

    Dichotic pitch: A new stimulus distinguishes normal and dyslexic auditory function

    Neuroreport

    (1998)
  • M. Erikson et al.

    The intelligibility of multiple talkers separated spatially in noise

  • S. Furukawa et al.

    Cortical representation of auditory space: Information-bearing features of spike patterns

    Journal of Neurophysiology

    (2002)
  • M.S. Gazzaniga et al.

    Cognitive Neuroscience

    (2002)
  • Cited by (44)

    • Ternary meter from spatial sounds: Differences in neural entrainment between musicians and non-musicians

      2019, Brain and Cognition
      Citation Excerpt :

      These results may indicate that our task does not clearly elicit any lateralized processing of meter for the spatial sounds. Another possibility for the lack of lateralization in the neural entrainment is that the right hemispheric bias (Brunetti et al., 2005; Johnson & Hautus, 2010; Kaiser et al., 2000; Zatorre & Penhune, 2001) for sound localization could have interacted with a lateralized processing of meter that masked any clear effect between the recordings of the right and left electrodes. Further analyses on source localization or comparing the topographies at each frequency of interest across conditions could possible reveal lateralization effects in meter induction on spatial sounds.

    View all citing articles on Scopus
    View full text