Elsevier

Neuropsychologia

Volume 80, 8 January 2016, Pages 79-89
Neuropsychologia

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

https://doi.org/10.1016/j.neuropsychologia.2015.11.008Get rights and content

Highlights

  • Patient MC has lesions including posterior temporal and parietal cortex.

  • MC has deficit in perception of sound motion direction in peripheral space.

  • Division of auditory motion processing into speed vs. direction.

  • Division of auditory motion processing into peripheral vs. central.

Abstract

It is still an open question if the auditory system, similar to the visual system, processes auditory motion independently from other aspects of spatial hearing, such as static location. Here, we report psychophysical data from a patient (female, 42 and 44 years old at the time of two testing sessions), who suffered a bilateral occipital infarction over 12 years earlier, and who has extensive damage in the occipital lobe bilaterally, extending into inferior posterior temporal cortex bilaterally and into right parietal cortex. We measured the patient's spatial hearing ability to discriminate static location, detect motion and perceive motion direction in both central (straight ahead), and right and left peripheral auditory space (50° to the left and right of straight ahead). Compared to control subjects, the patient was impaired in her perception of direction of auditory motion in peripheral auditory space, and the deficit was more pronounced on the right side. However, there was no impairment in her perception of the direction of auditory motion in central space. Furthermore, detection of motion and discrimination of static location were normal in both central and peripheral space. The patient also performed normally in a wide battery of non-spatial audiological tests. Our data are consistent with previous neuropsychological and neuroimaging results that link posterior temporal cortex and parietal cortex with the processing of auditory motion. Most importantly, however, our data break new ground by suggesting a division of auditory motion processing in terms of speed and direction and in terms of central and peripheral space.

Introduction

Dynamic properties of spatial sounds, such as sound motion, are salient aspects of the acoustic environment. Early on it has been questioned if the auditory system, like the visual system, processes motion independently from static location (e.g. Grantham, 1986). Evidence in favor of such a compartmentalization of the auditory system has been accumulating. For example, neuroimaging suggests that areas in temporal and parietal cortices are more active in the processing of auditory motion as compared to static location (e.g., Baumgart et al., 1999; Bremmer et al., 2001; Griffiths et al., 1994, 1998; Hall et al., 2003; Krumbholz et al., 2005; Lewis et al., 2000; Poirier et al., 2005; Saenz et al., 2008; Warren et al., 2002). Supporting evidence has also been reported using electroencephalography, EEG (Getzmann, 2011, Krumbholz et al., 2007), and transcranial magnetic stimulation, TMS (Lewald et al., 2011). There is additional neuropsychological evidence to suggest cortical specialization for auditory motion processing, such as reports of motion deafness after damage to temporal (Ducommun et al., 2004) or temporal and parietal brain areas (Griffiths et al., 1996, Lewald et al., 2009). Of particular relevance to our current report is the study by Lewald et al. (2009), who introduced three cases of hemispherectomy (two left, one right), all of whom showed severely impaired perception of motion direction combined with milder deficits in the perception of static location. Most interestingly, Lewald et al. (2009) also described a case with right anterior temporal lobectomy (case MB), who showed impaired processing of stationary location, whilst his ability to perceive motion direction was entirely normal. They proposed that the processing of stationary location may take place in more anterior parts of the temporal lobe (i.e. Heschl's gyrus, superior, middle and inferior temporal gyri and the temporal pole), whereas the processing of motion may take place in posterior parts of the temporal lobe and/or in the parietal cortex.

In the current study we introduce patient MC, who has bilateral lesions in posterior parts of the temporal lobe and in right parietal cortex (in addition to lesions in the occipital lobe). Thus, she has brain lesions that permit a direct test of the hypothesis that processing of stationary location may take place in more anterior parts of the temporal lobe, whereas processing of motion direction may take place in posterior parts of the temporal lobe and/or in the parietal cortex. Specifically, if the hypothesis put forth by Lewald et al. (2009) is true, MC should show a deficit in the perception of motion direction, but intact perception of stationary location, and in this way the behavioral data observed in MC and MB would form a double-dissociation.

Lewald et al. (2009) used a task in which participants had to judge the direction of motion in right and left peripheral auditory space (i.e. 50° to the left and right of straight ahead), and the location of a stationary sound in central auditory space (i.e. straight ahead). Thus, the nature of the perceptual judgment (i.e. judgment of motion direction vs. judgment of static location) was confounded with the part of auditory space in which the stimulus was presented (i.e. peripheral vs. central). Typically, people perform better when they are tested in central as compared to peripheral space (e.g. Blauert, 1997). Thus, to avoid confounding the nature of the perceptual judgment with the part of auditory space in which the stimulus is presented, we tested MC's ability to perceive motion direction and static location in central as well as right and left peripheral auditory space. In addition, we decided to test not only MC's perception of sound motion direction, but also her processing of sound motion speed (i.e. detection). The reasoning behind the latter manipulation was that for the processing of visual motion it has been suggested that separate mechanisms may be employed for the processing of direction and speed (e.g. Matthews and Qian, 1999; Matthews et al., 2001), and we wanted to explore if a similar separation might exist in the auditory domain. For example, if sound motion direction was processed separately from sound motion speed, one might observe a deficit in the perception of sound motion direction whilst perception of sound motion speed might be normal, or vice versa. In sum, here we tested perception of static location, motion speed and motion direction in both central and peripheral auditory space. Such a complete set of tests has not been conducted previously. To ensure that MC's non-spatial hearing ability was intact, we also conducted a wide array of non-spatial hearing tests.

Section snippets

Material and methods

Testing occurred on two separate occasions, approximately two years apart. For the first test occasion, patient MC and two control participants were tested at the University of Western Ontario, and the remaining five control participants were tested at Durham University. For the second test occasion MC was tested at her home, and seven control participants were tested at Durham University. Consent was obtained according to the Declaration of Helsinki. All testing procedures were approved by the

Non-spatial audiological tests

MC's performance in all non-spatial audiological tests was within the limits of normative samples. The part we consider diagnostic of brain stem function are DPOAE inhibition and ABRs. Importantly, DPOAE inhibition and all aspects of ABRs are normal, except for the inter‐aural latency difference for ABR wave III, which was larger than normal in MC (0.33 ms versus 0.17 ms). However, this could be due to asymmetry in the volume conductor (the electrical circuit followed by neural currents) since

Discussion

MC shows a highly selective impairment for the processing of sound motion direction in peripheral auditory space, which is more pronounced on the right side (i.e. on the right side both bias and threshold are outside normal range, whereas on the left side it is only her bias). Interestingly, on neither side of space is her deficit due to her responses being random, but rather she has a general tendency to perceive movements as being clockwise. On the left side this leads to a general shift of

Conclusion

The overall pattern of results we found in MC paints a picture of spatial hearing that is much more complex than previously assumed, and which not only differentiates between static location vs. motion, but that also differentiates between detection of motion speed and direction, and between central and peripheral space. Previous studies have not considered or investigated these distinctions, but they provide a fruitful avenue for further research into the organization of auditory spatial

Acknowledgments

We thank Markus Hausmann and two anonymous reviewers for comments on a previous version of this manuscript. This research was supported for grants from the Natural Sciences and Engineering Research Council of Canada CREATE Program (LT), Natural Sciences and Engineering Research Council of Canada Discovery Grants Program (249877–2006-RGPIN) (JCC), Natural Sciences and Engineering Research Council of Canada Discovery Grants Program (MD), SHARCNET Research Chairs Program (MD), Natural Sciences and

References (45)

  • P. Voss et al.

    Early-and late-onset blind individuals show supra-normal auditory abilities in far-space

    Curr. Biol.

    (2004)
  • J.D. Warren et al.

    Perception of sound-source motion by the human brain

    Neuron

    (2002)
  • F. Baumgart et al.

    A movement sensitive area in auditory cortex

    Nature

    (1999)
  • D. Bavelier et al.

    Cross-modal plasticity: where and how?

    Nat. Rev. Neurosci.

    (2002)
  • J. Blauert

    Spatial Hearing: The Psychophysics of Human Sound Localization

    (1997)
  • D.H. Brainard

    The psychophysics toolbox

    Spat. Vis.

    (1997)
  • H. Burton

    Visual cortex activity in early and late blind people

    J. Neurosci.

    (2003)
  • H.E. Burtt

    Auditory illusions of movement—a preliminary study

    J. Exp. Psychol.

    (1917)
  • J.C. Culham et al.

    Preserved processing of motion and dorsal stream functions in a patient with large bilateral lesions of occipitotemporal cortex

    J. Vis.

    (2008)
  • C.Y. Ducommun et al.

    Cortical motion deafness

    Neuron

    (2004)
  • W.G. Gardner et al.

    HRTF measurements of a KEMAR

    J. Acoust. Soc. Am.

    (1995)
  • S. Getzmann

    Auditory motion perception: onset position and motion direction are encoded in discrete processing stages

    Eur. J. Neurosci.

    (2011)
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