Diffusion Tensor Imaging Reveals White Matter Microstructure Correlations With Auditory Processing Ability

Department of Radiology, Pediatric Neuroimaging Research Consortium, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio 45229, USA.
Ear and hearing (Impact Factor: 2.84). 11/2010; 32(2):156-67. DOI: 10.1097/AUD.0b013e3181f7a481
Source: PubMed


Correlation of white matter microstructure with various cognitive processing tasks and with overall intelligence has been previously demonstrated. We investigate the correlation of white matter microstructure with various higher-order auditory processing tasks, including interpretation of speech-in-noise, recognition of low-pass frequency filtered words, and interpretation of time-compressed sentences at two different values of compression. These tests are typically used to diagnose auditory processing disorder (APD) in children. Our hypothesis is that correlations between white matter microstructure in tracts connecting the temporal, frontal, and parietal lobes, as well as callosal pathways, will be seen. Previous functional imaging studies have shown correlations between activation in temporal, frontal, and parietal regions from higher-order auditory processing tasks. In addition, we hypothesize that the regions displaying correlations will vary according to the task because each task uses a different set of skills.
Diffusion tensor imaging (DTI) data were acquired from a cohort of 17 normal-hearing children aged 9 to 11 yrs. Fractional anisotropy (FA), a measure of white matter fiber tract integrity and organization, was computed and correlated on a voxelwise basis with performance on the auditory processing tasks, controlling for age, sex, and full-scale IQ.
Divergent correlations of white matter FA depending on the particular auditory processing task were found. Positive correlations were found between FA and speech-in-noise in white matter adjoining prefrontal areas and between FA and filtered words in the corpus callosum. Regions exhibiting correlations with time-compressed sentences varied depending on the degree of compression: the greater degree of compression (with the greatest difficulty) resulted in correlations in white matter adjoining prefrontal (dorsal and ventral), whereas the smaller degree of compression (with less difficulty) resulted in correlations in white matter adjoining audiovisual association areas and the posterior cingulate. Only the time-compressed sentences with the lowest degree of compression resulted in positive correlations in the centrum semiovale; all the other tasks resulted in negative correlations.
The dependence of performance on higher-order auditory processing tasks on brain anatomical connectivity was seen in normal-hearing children aged 9 to 11 yrs. Results support a previously hypothesized dual-stream (dorsal and ventral) model of auditory processing, and that higher-order processing tasks rely less on the dorsal stream related to articulatory networks and more on the ventral stream related to semantic comprehension. Results also show that the regions correlating with auditory processing vary according to the specific task, indicating that the neurological bases for the various tests used to diagnose APD in children may be partially independent.

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Available from: Scott K Holland, Oct 10, 2015
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    • "Furthermore, behavioral tests most frequently utilized in the diagnosis of APD have been repeatedly criticized for relying on higher order processing constructs, including memory, language, and attention (Cacace and McFarland 2005, 2013; Moore 2006; Moore et al. 2010). A recent diffusion tensor imaging (DTI) study investigating the neural correlates of several behavioral tests used in the diagnosis of APD (Schmithorst et al. 2011), corroborated this concern by demonstrating that test performance correlated with independent white matter integrity in regions subserving higher order processing constructs. These findings cast doubt on the interpretation of abnormal behavioral task performance as indicative of pure sensory APD, since supramodal neural deficits may alternatively account for deficient performance. "
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    ABSTRACT: IntroductionThe purpose of the present study was to identify biomarkers of listening difficulties by investigating white matter microstructure in children suspected of auditory processing disorder (APD) using diffusion tensor imaging (DTI). Behavioral studies have suggested that impaired cognitive and/or attention abilities rather than a pure sensory processing deficit underlie listening difficulties and auditory processing disorder (APD) in children. However, the neural signature of listening difficulties has not been investigated.Methods Twelve children with listening difficulties and atypical left ear advantage (LEA) in dichotic listening and twelve age- and gender-matched typically developing children with typical right ear advantage (REA) were tested. Using voxel-based analysis, fractional anisotropy (FA), and mean, axial and radial diffusivity (MD, AD, RD) maps were computed and contrasted between the groups.ResultsListening difficulties were associated with altered white matter microstructure, reflected by decreased FA in frontal multifocal white matter regions centered in prefrontal cortex bilaterally and left anterior cingulate. Increased RD and decreased AD accounted for the decreased FA, suggesting delayed myelination in frontal white matter tracts and disrupted fiber organization in the LEA group. Furthermore, listening difficulties were associated with increased MD (with increase in both RD and AD) in the posterior limb of the internal capsule (sublenticular part) at the auditory radiations where auditory input is transmitted between the thalamus and the auditory cortex.Conclusions Our results provide direct evidence that listening difficulties in children are associated with altered white matter microstructure and that both sensory and supramodal deficits underlie the differences between the groups.
    Brain and Behavior 07/2014; 4(4). DOI:10.1002/brb3.237 · 2.24 Impact Factor
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    • "It must be expected, thus, that the visual system encompasses – to some extent – preconfigurated connections with the auditory system providing a basis for interactions between the two modalities. Indeed, a recent Diffusion Tensor Imaging study (DTI) – evaluating white matter parameters in children – found inter-subject differences in fractional anisotropy to correlate with the comprehension of time-compressed speech [73]: Moderately manipulated signals (40% compression) yielded these effects in white matter areas adjacent to audiovisual association cortex and posterior cingulate gyrus while a greater degree of compression resulted in changes of tracts adjoining prefrontal areas (dorsal and ventral). "
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    ABSTRACT: Individuals suffering from vision loss of a peripheral origin may learn to understand spoken language at a rate of up to about 22 syllables (syl) per second - exceeding by far the maximum performance level of normal-sighted listeners (ca. 8 syl / s). To further elucidate the brain mechanisms underlying this extraordinary skill, functional magnetic resonance imaging (fMRI) was performed in blind subjects of varying ultra-fast speech comprehension capabilities and sighted individuals while listening to sentence utterances of a moderately fast (8 syl / s) or ultra-fast (16 syl / s) syllabic rate. Besides left inferior frontal gyrus (IFG), bilateral posterior superior temporal sulcus (pSTS) and left supplementary motor area (SMA), blind people highly proficient in ultra-fast speech perception showed significant hemodynamic activation of right-hemispheric primary visual cortex (V1), contralateral fusiform gyrus (FG), and bilateral pulvinar (Pv). Presumably, FG supports the left-hemispheric perisylvian "language network", i.e., IFG and pSTS, during the (segmental) sequencing of verbal utterances whereas the collaboration of bilateral pulvinar, right auditory cortex, and ipsilateral V1 implements a signal-driven timing mechanism related to syllabic (suprasegmental) modulation of the speech signal. These data structures, conveyed via left SMA to the perisylvian "language zones", might facilitate -- under time-critical conditions -- the consolidation of linguistic information at the level of verbal working memory.
    BMC Neuroscience 07/2013; 14(1):74. DOI:10.1186/1471-2202-14-74 · 2.67 Impact Factor
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    • "Our results are therefore consistent with previous findings that ventral parietal cortex plays a pivotal role in language-based tasks [37, 55–57]. Inferior parietal activity has been found more reliably in studies of working memory than in those of explicit recall [15, 58–60], and our results are also consistent with these findings. Moreover, during the encoding phase of our study (Figure 1), right BA40 was activated at the time our spoken stimulus words were first encoded [39]. "
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    ABSTRACT: Attention is crucial for encoding information into memory, and current dual-process models seek to explain the roles of attention in both recollection memory and incidental-perceptual memory processes. The present study combined an incidental memory paradigm with event-related functional MRI to examine the effect of attention at encoding on the subsequent neural activation associated with unintended perceptual memory for spoken words. At encoding, we systematically varied attention levels as listeners heard a list of single English nouns. We then presented these words again in the context of a recognition task and assessed the effect of modulating attention at encoding on the BOLD responses to words that were either attended strongly, weakly, or not heard previously. MRI revealed activity in right-lateralized inferior parietal and prefrontal regions, and positive BOLD signals varied with the relative level of attention present at encoding. Temporal analysis of hemodynamic responses further showed that the time course of BOLD activity was modulated differentially by unintentionally encoded words compared to novel items. Our findings largely support current models of memory consolidation and retrieval, but they also provide fresh evidence for hemispheric differences and functional subdivisions in right frontoparietal attention networks that help shape auditory episodic recall.
    International Journal of Biomedical Imaging 01/2012; 2012:579786. DOI:10.1155/2012/579786
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