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Scientific Understanding of Consciousness |
Auditory Cortices Phonetic Representation and Left Frontal Phonological Processing
Science 6 December 2013: Vol. 342 no. 6163 pp. 1251-1254 Intact But Less Accessible Phonetic Representations in Adults with Dyslexia Bart Boets, Hans P. Op de Beeck, Maaike Vandermosten, Sophie K. Scott, Céline R. Gillebert, Dante Mantini, Jessica Bulthé, Stefan Sunaert, Jan Wouters, Pol Ghesquière 1Child and Adolescent Psychiatry, KU Leuven, 3000 Leuven, Belgium. 2Parenting and Special Education Research Unit, KU Leuven, 3000 Leuven, Belgium. 3Laboratory of Biological Psychology, KU Leuven, 3000 Leuven, Belgium. 4Institute of Cognitive Neuroscience, University College London, London WC1N 3AR, UK. 5Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, UK. 6Department of Health Sciences and Technology, ETH Zürich, 8092 Zürich, Switzerland. 7Department of Radiology, KU Leuven, 3000 Leuven, Belgium. 8ExpORL, Department of Neurosciences, KU Leuven, 3000 Leuven, Belgium. [paraphrase] Dyslexia is a severe and persistent reading and spelling disorder caused by impairment in the ability to manipulate speech sounds. We combined functional magnetic resonance brain imaging with multivoxel pattern analysis and functional and structural connectivity analysis in an effort to disentangle whether dyslexics’ phonological deficits are caused by poor quality of the phonetic representations or by difficulties in accessing intact phonetic representations. We found that phonetic representations are hosted bilaterally in primary and secondary auditory cortices and that their neural quality (in terms of robustness and distinctness) is intact in adults with dyslexia. However, the functional and structural connectivity between the bilateral auditory cortices and the left inferior frontal gyrus (a region involved in higher-level phonological processing) is significantly hampered in dyslexics, suggesting deficient access to otherwise intact phonetic representations. Speech perception involves the mapping of spectrally complex and rapidly changing acoustic signals onto discrete and abstract phonetic sound categories or phonemes. Developmental dyslexia is a hereditary neurological disorder characterized by severe and persistent reading and/or spelling impairments. Individuals with dyslexia perform poorly on tasks that require phonological awareness, verbal short-term memory, and lexical access. Performance on these phonological tasks predicts reading acquisition in both normal and dyslexic readers. One view is that success on these tasks reflects the quality of underlying phonological (phonetic) representations and that these representations of speech sounds are distorted or less well specified in individuals with dyslexia. An alternative view holds that in people with dyslexia, representations are intact but access to the representations is problematic. Here, we combined functional magnetic resonance imaging (fMRI) with multivoxel pattern analysis (MVPA) and functional and structural connectivity analysis to disentangle whether dyslexia is caused by poor quality of the phonetic representation or by difficulty in accessing an intact representation. We collected whole-brain functional images in 23 adults with a diagnosis of dyslexia and 22 matched normal readers while they listened to different versions of four sublexical speech sounds and performed an easy phoneme discrimination task. The selection of stimuli allowed us to investigate both vowel and stop-consonant discrimination, which rely on spectral and spectrotemporal acoustic feature processing, respectively. If dyslexia is related to a deficit in the quality of phonetic representations, then we expect that the neural representations would be less robust and distinct in individuals with dyslexia than in normal readers. Given dyslexics’ particular problems processing temporal cues, such as those involved in consonant discrimination, we expected the most prominent group differences for neural patterns distinguishing between consonants. We analyzed the pattern of multivoxel activity within six left-hemisphere and six right-hemisphere regions involved in speech processing and within one non–speech control region (primary visual cortex V1). We found significant differences between the four phonetic comparisons in bilateral primary auditory cortex (PAC), superior temporal gyrus (STG), middle temporal gyrus (MTG), and supramarginal gyrus (SMG) (Ps < 0.0003), and unilaterally in right angular gyrus (AG) and right inferior frontal gyrus (IFG) (Ps < 0.03). Across all regions and for both reading groups, left-hemisphere regions were significantly more sensitive than right-hemisphere regions to differences in consonants (P = 0.017). We found no lateralization for vowel decoding in either normal or dyslexic readers (F < 1). This analysis confirmed that phonetic representations are primarily hosted bilaterally in primary and secondary auditory cortices and that both normal and dyslexic readers shared similar quality of these representations. Attention may modulate brain activity and alter brain activity profiles. As these stimuli were processed less intentionally, they yielded less brain activity. Nonetheless, even under this more stringent condition, speech sounds could be differentiated in left and right PAC, STG, MTG, and SMG (Ps < 0.05). We found no difference in the neural quality of phonetic representations between dyslexic and normal readers. Several studies have shown that Broca’s area, particularly the left IFG pars opercularis, is involved in sensory-motor integration and effortful phonological processing. Hence, this area, which itself does not host phonetic representations, must access the representations in primary and secondary auditory cortices to compute the required phonological manipulations. We investigated the efficiency of access or the quality of interregional brain communication by assessing intrinsic functional connectivity between each possible pairing of the 13 anatomical regions. At a neuroanatomical level, adequate communication between left IFG and left STG is effected by the left arcuate fasciculus, the major language tract that ensures an efficient signal transmission between Wernicke’s and Broca’s areas. We recently collected diffusion tensor imaging data in a subsample (N = 32) of our participants and delineated the left arcuate fasciculus and its three constituent segments (direct, anterior, and posterior) on the basis of whole-brain tractography. For the present report, we complemented these data and analyses to comprise the full sample (N = 45). Group comparisons revealed significantly reduced white matter integrity of the left arcuate fasciculus in dyslexics (P = 0.019), in particular in the segment that directly connects posterior temporal and frontal areas (P = 0.038); this result provides neuroanatomical evidence that corroborates the deficiency in functional connectivity between left IFG and left STG. The functional and structural connectivity measures were not mutually related (r = 0.06, P = 0.70). This is in line with recent evidence highlighting the differences between the two types of connectivity measures and suggests that both measures are complementary, each capturing a different aspect of the communication between left frontal and temporal language areas. Together, the functional and structural connectivity measures accounted for 35% of the variance in reading and spelling ability, and they predicted reading status (dyslexic versus normal reader) with an accuracy of 73%. This finding adds to the growing recognition of dyslexia as a disconnection syndrome. Our results indicate that deficient phonetic representations are not the core problem in dyslexia. Does this imply that it is time to abandon the influential phonological deficit hypothesis? No, certainly not. The behavioral data of our dyslexic participants reveal that they do show severe deficits in the traditional phonological domains, including phonological awareness, verbal short-term memory, and lexical access. Yet our neuroimaging findings suggest that it is not a deficit in underlying representations that characterizes dyslexia. Instead, our results suggest that a dysfunctional connection between frontal and temporal language areas impedes efficient access to otherwise intact representations of speech sounds, thus hampering a person’s ability to manipulate them fluently. [end of paraphrase]
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