Elsevier

NeuroImage

Volume 55, Issue 3, 1 April 2011, Pages 891-899
NeuroImage

Spatiotemporal signatures of an abnormal auditory system in stuttering

https://doi.org/10.1016/j.neuroimage.2010.12.083Get rights and content

Abstract

People who stutter (PWS) can reduce their stuttering rates under masking noise and altered auditory feedback; such a response can be attributed to altered auditory input, which suggests that abnormal speech processing in PWS results from abnormal processing of auditory input. However, the details of this abnormal processing of basic auditory information remain unclear. In order to characterize such abnormalities, we examined the functional and structural changes in the auditory cortices of PWS by using a 306-channel magnetoencephalography system to assess auditory sensory gating (P50m suppression) and tonotopic organization. Additionally, we employed voxel-based morphometry to compare cortical gray matter (GM) volumes on structural MR images. PWS exhibited impaired left auditory sensory gating. The tonotopic organization in the right hemisphere of PWS is expanded compared with that of the controls. Furthermore, PWS showed a significant increase in the GM volume of the right superior temporal gyrus, consistent with the right tonotopic expansion. Accordingly, we suggest that PWS have impaired left auditory sensory gating during basic auditory input processing and that some error signals in the auditory cortex could result in abnormal speech processing. Functional and structural reorganization of the right auditory cortex appears to be a compensatory mechanism for impaired left auditory cortex function in PWS.

Research Highlights

► People who stutter (PWS) exhibited impaired left auditory sensory gating. ► The right tonotopic organization of PWS expanded compared with that of controls. ► In VBM, PWS had a significant increase of the right superior temporal gyrus. ► The increment in VBM is consistent with right tonotopic expansion.

Introduction

Stuttering is a developmental disorder that affects speech fluency. This disorder is observed in 5% of children aged between 2 and 4 years (Månsson, 2000). The mechanism of stuttering is still a matter of debate. People who stutter (PWS) decrease their stuttering rates temporarily under masking noise and altered auditory feedback, which is not only because of the resulting slower speech rate but also because of altered auditory input (Altrows and Bryden, 1977, Kalinowski et al., 1993, Lincoln et al., 2006, Hampton and Weber-Fox, 2008). This suggests that auditory input processing could be different in PWS compared with non-stuttering subjects. Postma and Kolk (1992) proposed “auditory feedback defect theories in PWS,” in which PWS have deviant error monitoring of speech production, namely, PWS detect errors more than people who do not stutter. Postma and Kolk, 1993, Postma, 2000 also proposed “the covert repair hypothesis,” in which stuttering derives from the need to repeatedly repair errors before and after speech motor movement. Thereafter, Max et al. (2004) proposed “internal models and feedback-biased motor control theory”. In this hypothesis, a motor plan is constructed and executed by a feedforward controller, and execution is adjusted by a feedback controller that integrates in real time both afferent (auditory) and efferent (motor) signals. They speculated that stuttering resulted from a mismatch between predicted (feedforward) and actual (feedback) consequences of the executed movements. Overall, stuttering could be related to impaired auditory–motor integration.

Fox et al. (1996) performed neuroimaging studies and reported that stuttering is a disorder of integration within the speech system and not of a single area. Subsequently, stutter-typical networks are not only involved in an extended right-hemispheric network, including the frontal operculum, the temporo-parietal junction, and the dorsolateral prefrontal cortex (Kell et al., 2009), but also in the impaired left-hemispheric network, including the arcuate fasciculus (Sommer et al., 2002, Chang et al., 2008, Watkins et al., 2008, Cykowski et al., 2010), which connects temporal regions with frontal speech motor-planning (including Broca's area) and motor regions, as well as the striato-thalamico-cortico-striatal loop, which has important connections to the auditory regions (Giraud et al., 2008). Additionally, Chang et al. (2008) identified bilaterally abnormal fractional anisotropy in the corticospinal/corticobulbar tract (which is involved in speech motor control) and in a posterior-lateral region underlying the supramarginal gyrus (rostral portion of the inferior parietal lobe that is connected to the classic frontotemporal language areas) in stuttering children. Watkins et al. (2008) also found disturbed integrity of the white matter underlying the functional underactive areas in the ventral premotor cortex (a connection with posterior-superior temporal and inferior parietal cortex), which provides a substrate for the integration of articulatory planning and sensory feedback. Fluency-shaping therapies reduce right hemispheric over-activation, normalize basal ganglia activity and reactivate left-hemispheric cortex (De Nil et al., 2003, Neumann et al., 2005, Giraud et al., 2008, Kell et al., 2009). Taken together, abnormal auditory–motor integration can be the neural basis of stuttering.

Auditory–motor integration has been investigated in 2 magnetoencephalographic (MEG) studies (Salmelin et al., 1998, Beal et al., 2010). Salmelin et al. (1998) recorded auditory evoked magnetic fields to a single pure tone during the performance of 4 language-related tasks (reading silently, mouth movements only, reading aloud, and reading in chorus with another person). They found that the interhemispheric balance of the N100m responses of PWS was affected more severely by the tasks involving speech than by the 2 non-verbal tasks. Beal et al. (2010) reported the phenomenon of speech-induced suppression of the auditory N100m for vowel stimuli and showed that both the P50m and N100m were suppressed for word stimuli. They also revealed that the P50m and N100m latencies in PWS were significantly longer than those in the controls, which suggested that the timing of cortical auditory processing in PWS was slower than that in controls under various stimuli. These findings support the altered auditory–motor integration in PWS.

Therefore, we hypothesized that PWS have an abnormal auditory–motor integration system. We tested our hypothesis by using auditory sensory gating that modulates auditory inputs and tonotopic organization that corresponds to auditory inputs. PWS do not have abnormal auditory inputs to brainstem responses (Decker et al., 1982, Newman et al., 1985, Stager, 1990). To validate our hypothesis, we conducted 3 experiments. First, we examined auditory sensory gating by MEG using a P50m (or P50 in EEG) suppression standard paradigm, as has been used in studies on schizophrenia and Alzheimer's disease (Adler et al., 1982, Jessen et al., 2001, Thoma et al., 2003, Hirano et al., 2010). We presented 2 successive click sounds to the subjects monaurally, and the lack of P50m suppression in response to the second sound suggested an inability to filter unnecessary auditory information. Second, we measured the most frequently used N100m in response to 3 tonal stimuli at 250, 1000, and 4000 Hz to elucidate the expansion of the tonotopic map (Pantev et al., 1998b, Naka et al., 1999). MEG has both high spatial and temporal resolution and can be used to evaluate the differences in tonotopic organization in both auditory cortices of PWS and controls. Third, we performed three-dimensional voxel-based morphometry (VBM) to assess structural changes in the auditory cortex. Using the results of these studies, we have provided electrophysiological and structural evidence for abnormal auditory processing in PWS.

Section snippets

Subjects

Seventeen men who stutter (mean age, 30.2 ± 5.7 years; range, 21–41 years) and 18 control male subjects (mean age, 30.6 ± 6.2 years; range, 22–43 years) participated in the present study. PWS were recruited from a self-help group as volunteers and were diagnosed as having developmental stuttering according to DSM-IV (Diagnostic and Statistical Manual of Mental Disorders-IV). All subjects gave their written informed consent for participation in the study, and the study was approved by the Ethics

Experiment 1: Auditory sensory gating

In both groups, 2 successive clicks evoked a well-defined P50m response in the hemisphere contralateral to the stimulated ear (Fig. 1). Fig. 1A shows the data from 70 channels around the sensor with a maximal amplitude of P50m in the left hemisphere. Figs. 1B and C show the representative waveforms of P50m in a normal control and a stuttering subject, respectively. The amplitude of S2-P50m was apparently smaller than that of S1-P50m in the control subjects; however, no such amplitude difference

Discussion

We examined spatiotemporal signatures of the basic auditory system by using an auditory sensory gating paradigm and tonotopic maps with MEG and determined structural volumes by using VBM. The new findings of this study are summarized as impaired auditory sensory gating in the left hemisphere, functional map expansion of the right STG, and greater asymmetric tonotopic organization in PWS. We also found left-lateralized auditory sensory gating in normal controls.

Conclusions

Our study demonstrated that the disturbed auditory sensory gating in the left hemisphere is an electrophysiological signature of stuttering, which reflects an inability of PWS to gate out unnecessary auditory information and the consequent stuttering. We also indicated an increase in GM in the right auditory cortex corresponding to the expansion of tonotopic organization. Our findings further suggest that altered auditory information processing provides a clue about stuttering pathophysiology.

Acknowledgments

This work was supported by a Grant-in-Aid for Japan Society for the Promotion of Science (JSPS) Fellows (Y. K.) and by a Grant-in-Aid for Young Scientists (B) (K. O.).

References (71)

  • L.F. De Nil et al.

    A positron emission tomography study of short- and long-term treatment effects on functional brain activation in adults who stutter

    J. Fluency Disord.

    (2003)
  • T.N. Decker et al.

    Brainstem auditory electrical response characteristics of stutterers and nonstutterers: a preliminary report

    J. Fluency Disord.

    (1982)
  • J.C. Edgar et al.

    Interpreting abnormality: an EEG and MEG study of P50 and the auditory paired-stimulus paradigm

    Biol. Psychol.

    (2003)
  • A.L. Giraud et al.

    Severity of dysfluency correlates with basal ganglia activity in persistent developmental stuttering

    Brain Lang.

    (2008)
  • A. Hampton et al.

    Non-linguistic auditory processing in stuttering: evidence from behavior and event-related brain potentials

    J. Fluency Disord.

    (2008)
  • Y. Hirano et al.

    Auditory sensory gating to the human voice: a preliminary MEG study

    Psychiatry Res.

    (2008)
  • Y. Hirano et al.

    Auditory gating deficit to human voices in schizophrenia: a MEG study

    Schizophr. Res.

    (2010)
  • O. Korzyukov et al.

    Generators of the intracranial P50 response in auditory sensory gating

    Neuroimage

    (2007)
  • M. Lincoln et al.

    Altered auditory feedback and the treatment of stuttering: a review

    J. Fluency Disord.

    (2006)
  • C. Lu et al.

    Altered effective connectivity and anomalous anatomy in the basal ganglia-thalamocortical circuit of stuttering speakers

    Cortex

    (2010)
  • H. Månsson

    Childhood stuttering incidence and development

    J. Fluency Disord.

    (2000)
  • D. Naka et al.

    Structure of the auditory evoked magnetic fields during sleep

    Neuroscience

    (1999)
  • K. Neumann et al.

    Cortical plasticity associated with stuttering therapy

    J. Fluency Disord.

    (2005)
  • P.W. Newman et al.

    Brain stem electrical responses of stutterers and normals by sex, ears, and recovery

    J. Fluency Disord.

    (1985)
  • R.C. Oldfield

    Assessment and analysis of handedness — Edinburgh inventory

    Neuropsychologia

    (1971)
  • T. Onitsuka et al.

    The effect of interstimulus intervals and between-block rests on the auditory evoked potential and magnetic field: is the auditory P50 in humans an overlapping potential?

    Clin. Neurophysiol.

    (2000)
  • C. Pantev et al.

    Specific tonotopic organizations of different areas of the human auditory-cortex revealed by simultaneous magnetic and electric recordings

    Electroencephalogr. Clin. Neurophysiol.

    (1995)
  • A. Postma

    Detection of errors during speech production: a review of speech monitoring models

    Cognition

    (2000)
  • D.C. Rojas et al.

    Alterations in tonotopy and auditory cerebral asymmetry in schizophrenia

    Biol. Psychiatry

    (2002)
  • M. Sommer et al.

    Disconnection of speech-relevant brain areas in persistent developmental stuttering

    Lancet

    (2002)
  • S.V. Stager

    Heterogeneity in stuttering: results from auditory brainstem response testing

    J. Fluency Disord.

    (1990)
  • B.J. Weiland et al.

    Evidence for a frontal cortex role in both auditory and somatosensory habituation: a MEG study

    Neuroimage

    (2008)
  • L.E. Adler et al.

    Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia

    Biol. Psychiatry

    (1982)
  • D.S. Beal et al.

    Voxel-based morphometry of auditory and speech-related cortex in stutterers

    NeuroReport

    (2007)
  • E. Conture

    Stuttering: Its Nature, Diagnosis and Treatment

    (2001)
  • Cited by (57)

    • Auditory temporal processing assessment in children with developmental stuttering

      2020, International Journal of Pediatric Otorhinolaryngology
    View all citing articles on Scopus
    View full text