Marjorie Dole, Fanny Meunier, Michel Hoen
INSERM U1028, CNRS UMR5292, Lyon Neuroscience Research Centre, Brain Dynamics and Cognition Team, Lyon F-69500, France
Keywords: Dyslexia, Asymmetry, VBM, Superior temporal gyrus, Speech-in-noise
Abstract
In the present study, we investigated morphological characteristics of the dyslexic brain.
Dyslexia is a developmental disorder affecting the acquisition of reading and spelling abilities, associated with a phonological deficit. Speech perception disabilities are also frequently observed, particularly in challenging conditions, when masked by noise for example. These deficits have clear neurobiological correlates, such as a reduction in functional activation and modifications of functional asymmetry in cortical regions involved in speech processing, such as superior temporal regions. These functional deficits are associated with morphological abnormalities which, amongst other, manifest themselves by a reduction in gray and white matter volume together with modifications of the leftward asymmetry in the superior temporal regions. Although consistently observed, these differences in cerebral asymmetry and their relation with the behavioral deficits, particularly the speech-in-noise problem, are not yet fully understood. The purpose of our study was to investigate gray/white matter asymmetries in dyslexic adults using automated image processing, derived from the VBM technique. Moreover correlations with speech-in-noise perception abilities were also investigated. Our results confirm the presence of gray and white matter distribution abnormalities in the superior temporal gyrus (STG) in dyslexics. In particular, primary auditory cortex was less asymmetric in dyslexics, an observation that could be related to their speech-in-noise comprehension difficulties. Secondary auditory areas were also found to be less asymmetric in dyslexics. Finally this was associated with a reduction in gray and white matter volume in more anterior regions of the STG/STS, which have previously been linked with the processing of masked speech. Taken together, these results provide further understanding about morphological alterations in the dyslexic brain, by highlighting the presence of both gray and white matter deficit at the early stage of auditory processing, and their potential involvement in the speech-in-noise deficit.
Chapitre 2D. Asymétries et perception de la parole dans le bruit chez le sujet dyslexique
Page 186
Introduction
Dyslexia is a neurodevelopmental disorder affecting the acquisition of reading and spelling abilities in the absence of any other neurological disorder and in spite of normal intelligence and favorable socio-educational environment. Although being a developmental disorder, difficulties associated with dyslexia are long-lasting and remain at adult age [1,2]. The current consensus in the literature holds that dyslexic children present a deficit in the processing of phonological information preventing efficient acquisition of phoneme-to-grapheme conversion rules and disturbing the learning of reading and spelling. This phonological deficit manifests itself through reduced performances in tasks involving phonological processing, such as phonological awareness [3,4], different aspects of verbal memory [5], repetition of complex pseudowords or rare words [3,6] or rapid automatized naming [7,8]. Associated with this phonological deficit, speech perception deficits have also been demonstrated in dyslexia. Although this remains difficult to demonstrate in optimal quiet conditions, the results are highly replicable as soon as speech must be perceived in challenging conditions, when masked by noise for example [9-13]. Recently, by presenting speech in different backgrounds and in different listening configurations, we showed that the severity of this difficulty is highly dependent on the type of noise used as background and the listening configuration tested [14]. In this experiment, the speech-in-noise comprehension deficit of adult dyslexics was particularly marked when the concurrent sound was speech compared to other speech-derived noises. This observation reinforces the hypothesis of a specific difficulty with the processing of speech information in dyslexia. In the present study, we will explore the specificities of gray and white matter in dyslexic brains and their links to speech-in-noise comprehension abilities.
If a consensus is emerging regarding behavioral difficulties observed in the context of dyslexia, the cerebral bases of these deficits still constitute a largely debated issue, even if numerous neuroimaging experiments tend to show a clear link between behavioral deficits and underlying cerebral dysfunction. When investigating cortical abnormalities underlying dyslexia, one recurrent finding is the presence of abnormal asymmetry patterns both at the functional and morphological levels. Morphological abnormalities in dyslexic participants are usually observed in reading and speech processing regions [15] and abnormal activation patterns are generally associated with alterations of the left-right functional asymmetry in the same regions [16,17]. Functional anomalies most often consist in activation deficits in brain regions engaged in reading and speech processing, such as the superior, medial and inferior temporal gyri, inferior frontal gyrus (IFG), and fusiform gyrus [18-21]. Atypical functional asymmetry patterns have also been observed at primary stages of auditory processing pathways such as in the auditory brainstem [22] or in the primary auditory cortex. Using magnetoencephalography (MEG), for example, Heim et al. [23] reported an abnormal asymmetry of the P100m evoked in response to the presentation of a /ba/ syllable in dyslexic children and adolescents. P100m generators were found to be leftward
Chapitre 2D. Asymétries et perception de la parole dans le bruit chez le sujet dyslexique
asymmetric in normal readers but symmetric in dyslexics. This observation was subsequently confirmed by the same authors who found a similar pattern of results for the N100m generators in dyslexic adults [24]. More recently and in the framework of the asymmetric sampling in time (AST) theory [25,26], evidence of an alteration of asymmetric sampling in auditory cortices was reported in dyslexics. Reduced entrainment for rapid modulations in the left auditory cortex was reported, potentially resulting in impaired extraction of phonemic cues in the left hemisphere [27]. In the same study, the right auditory cortex of dyslexic participants exhibited enhanced entrainment to rapid modulations. Reinforcing the idea of a close link between atypical functional asymmetries in the dyslexic brain and the development of deficient phonological abilities, several studies demonstrated that a functional re-asymmetrisation of the auditory system could be stimulated in dyslexics following phonological training, with measurable effects both at the cortical [28] and peripheral levels [22].
According to former anatomical works these functional asymmetry abnormalities could be attributed to underlying morphological anomalies, as suggested by the pioneering research of Galaburda’s group [29,30]. These authors reported the presence of ectopias and dysplasias over left perisylvian regions of dyslexic brains, associated with a reduction of the leftward volumetric asymmetry of the planum temporale. These first observations were later confirmed using MR imaging [31-33], even if the question of the planum temporale’s asymmetry in dyslexia is still debated [34-38]. Nevertheless, atypical morphological asymmetry in dyslexia was also found outside the planum temporale. Dalby et al. [39], for example, performed manual measurements of the whole temporal lobe volumes and found reduced leftward asymmetry in dyslexic participants in comparison with normal readers. In 16 young dyslexic adults and 14 age-matched normal readers, Robichon et al. [37] measured cortical asymmetries in several language-related areas, including the planum temporale, IFG, and posterior parietal gyrus. They failed to find reduced asymmetry of the planum temporale, but found increased leftward asymmetry in parietal regions including parietal operculum and increased rightward asymmetry in Broca’s area inversely correlated to performances in a non-word reading task. More recently, voxel-based morphometry (VBM), a morphometric technique allowing separation of gray matter (GM) and white matter (WM) volumes has been used for investigating morphological abnormalities in dyslexia. VBM has also the advantage of being an automated image processing method, which prevents from errors typically associated with manual measurements thus leading to more accurate analyses [40]. In general, these studies confirmed the presence of abnormalities in temporal regions involved in speech processing and reading. Brambati et al. [41] for example, found reduced GM volumes bilaterally in the planum temporale, fusiform gyrus, and in the left inferior and superior temporal gyri and right middle temporal gyrus (MTG). Gray matter volume changes in left and/or right temporal regions were confirmed by several studies [42-45]. Exploring associated WM abnormalities in the dyslexic brain, several studies showed reductions of volume/density in the arcuate fasciculus including regions in Broca’s area and
Chapitre 2D. Asymétries et perception de la parole dans le bruit chez le sujet dyslexique
Page 188
temporal cortex [43-46]. The majority of studies specifically investigating WM in dyslexia used diffusion tensor imaging (DTI) and produced further arguments for the presence of WM deficits in these regions [46-49]. Although none of these studies were specifically designed to test WM asymmetries in dyslexia, some of them suggest a reduced leftward asymmetry of WM due to decreased volume or connectivity in the left hemisphere of dyslexic participants [43,46,48]. The presence of white matter deficits has given rise to the theory of a disconnection syndrome in dyslexia. According to this theory a disconnection between the language- and reading-related cortical areas would impair the communication between them, resulting in the observed cortical activation deficits and consequently in the associated behavioral impairments [43,47,50].
Taken together, these results provide a better understanding of the cortical mechanisms underlying the dyslexic syndrome. However, the question of anatomical asymmetries in temporal regions and their relation with behavioral deficits consistently observed in dyslexia is still far from clear. The aim of the present study is to compare asymmetry patterns of gray and white matter volumes in superior temporal regions in dyslexic adults and matched normal readers and examine the relation between these asymmetries and behavioral deficits typically associated with dyslexia. To explore these issues we used VBM to analyze GM and WM asymmetries in order to examine differences between adults with dyslexia and matched normal readers. To our knowledge, it is the first time that such automated asymmetry analyses are used in the context of dyslexia. Correlations between these asymmetry changes and scores obtained in a speech-in-noise perception task were also investigated. Finally standard VBM analyses were also performed in order to complete our observations and better understand to what extent GM/WM volume in each hemisphere contribute to the observed asymmetry differences.