Asymmetry of planum temporale constrains interhemispheric language plasticity in children with focal epilepsy.
ABSTRACT: Reorganization of eloquent cortex enables rescue of language functions in patients who sustain brain injury. Individuals with left-sided, early-onset focal epilepsy often show atypical (i.e. bilateral or right-sided) language dominance. Surprisingly, many patients fail to show such interhemispheric shift of language despite having major epileptogenic lesions in close proximity to eloquent cortex. Although a number of epilepsy-related factors may promote interhemispheric plasticity, it has remained unexplored if neuroanatomical asymmetries linked to human language dominance modify the likelihood of atypical lateralization. Here we examined the asymmetry of the planum temporale, one of the most striking asymmetries in the human brain, in relation to language lateralization in children with left-sided focal epilepsy. Language functional magnetic resonance imaging was performed in 51 children with focal epilepsy and left-sided lesions and 36 healthy control subjects. We examined the association of language laterality with a range of potential clinical predictors and the asymmetry of the length of the planum temporale. Using voxel-based methods, we sought to determine the effect of lesion location (in the affected left hemisphere) and grey matter density (in the unaffected right hemisphere) on language laterality. Atypical language lateralization was observed in 19 patients (38%) and in four controls (11%). Language laterality was increasingly right-sided in patients who showed atypical handedness, a left perisylvian ictal electroencephalographic focus, and a lesion in left anterior superior temporal or inferior frontal regions. Most striking was the relationship between rightward asymmetry of the planum temporale and atypical language (R = 0.70, P < 0.0001); patients with a longer planum temporale in the right (unaffected) hemisphere were more likely to have atypical language dominance. Voxel-based regression analysis confirmed that increased grey matter density in the right temporo-parietal junction was correlated with right hemisphere lateralization of language. The length of the planum temporale in the right hemisphere was the main predictor of language lateralization in the epilepsy group, accounting for 48% of variance, with handedness accounting for only a further 5%. There was no correlation between language lateralization and planum temporale asymmetry in the control group. We conclude that asymmetry of the planum temporale may be unrelated to language lateralization in healthy individuals, but the size of the right, contra-lesional planum temporale region may reflect a 'reserve capacity' for interhemispheric language reorganization in the presence of a seizure focus and lesions within left perisylvian regions.
Project description:In humans, both language and fine motor skills are associated with left-hemisphere specialization, whereas visuospatial skills are associated with right-hemisphere specialization. Individuals with autism spectrum conditions (ASC) show a profile of deficits and strengths that involves these lateralized cognitive functions. Here we test the hypothesis that regions implicated in these functions are atypically rightward lateralized in individuals with ASC and, that such atypicality is associated with functional performance. Participants included 67 male, right-handed adults with ASC and 69 age- and IQ-matched neurotypical males. We assessed group differences in structural asymmetries in cortical regions of interest with voxel-based analysis of grey matter volumes, followed by correlational analyses with measures of language, motor and visuospatial skills. We found stronger rightward lateralization within the inferior parietal lobule and reduced leftward lateralization extending along the auditory cortex comprising the planum temporale, Heschl's gyrus, posterior supramarginal gyrus, and parietal operculum, which was more pronounced in ASC individuals with delayed language onset compared to those without. Planned correlational analyses showed that for individuals with ASC, reduced leftward asymmetry in the auditory region was associated with more childhood social reciprocity difficulties. We conclude that atypical cerebral structural asymmetry is a potential candidate neurophenotype of ASC.
Project description:The goal of this study was to explore the structural correlates of functional language dominance by directly comparing the brain morphology of healthy subjects with left- and right-hemisphere language dominance.Twenty participants were selected based on their language dominance from a cohort of subjects with known language lateralization. Structural differences between both groups were assessed by voxel-based morphometry, a technique that automatically identifies differences in the local gray matter volume between groups using high-resolution T1-weighted magnetic resonance images.The main findings can be summarized as follows: (1) Subjects with right-hemisphere language dominance had significantly larger gray matter volume in the right hippocampus than subjects with left-hemisphere language dominance. (2) Leftward structural asymmetries in the posterior superior temporal cortex, including the planum temporale (PT), were observed in both groups.Our study does not support the still prevalent view that asymmetries of the PT are related in a direct way to functional language lateralization. The structural differences found in the hippocampus underline the importance of the medial temporal lobe in the neural language network. They are discussed in the context of recent findings attributing a critical role of the hippocampus in the development of language lateralization.
Project description:Background. An apparent paradox in the field of neuropsychology is that people with atypical cerebral lateralization do not appear to suffer any cognitive disadvantage, yet atypical cerebral lateralization is more common in children and adults with developmental language disorders. This study was designed to explore possible reasons for this puzzling pattern of results. Methods. We used functional transcranial Doppler ultrasound (fTCD) to assess cerebral blood flow during language production in 57 four-year-olds, including 15 children who had been late-talkers when first seen at 20 months of age. We categorized cerebral lateralization as left, right or bilateral, and compared proportions with each type of laterality with those seen in a previously tested sample of children aged 6-16 years. We also compared language scores at 4 years for those with typical and atypical lateralization, and then looked at the association the opposite way: comparing those with typical or impaired language in terms of their cerebral lateralization. Results. The distribution of types of cerebral lateralization was similar for 4-year-olds to that seen in older children. Overall, cerebral lateralization was not predictive of language level. However, for children who had language difficulties at 20 months and/or 4 years (N = 21), there was no population bias to left-hemisphere language activation, whereas children without language problems at either age showed a pronounced bias to left-sided language lateralization. Nevertheless, many children with right hemisphere language had no indications of language difficulties, confirming that atypical cerebral asymmetry is not a direct cause of problems. Conclusions. We suggest that atypical lateralization at the individual level is not associated with language impairment. However, lack of lateralization at the population level is a marker of risk for language impairment, which could be due to genetic or non-genetic causes.
Project description:<h4>Purpose</h4>determine if language disorder in children with autistic disorder (AD) corresponds to abnormalities in hemispheric asymmetries in auditory language cortex.<h4>Methods</h4>MRI morphometric study in children with AD (n = 50) to assess hemispheric asymmetries in auditory language cortex. A key region of interest was the planum temporale (PT), which is larger in the left hemisphere in most healthy individuals.<h4>Results</h4>(i) Heschl's gyrus and planum polare showed typical hemisphere asymmetry patterns; (ii) posterior Superior Temporal Gyrus (pSTG) showed significant rightward asymmetry; and (iii) PT showed a trend for rightward asymmetry that was significant when constrained to right-handed boys (n = 30). For right-handed boys, symmetry indices for pSTG were significantly positively correlated with those for PT. PT asymmetry was age dependent, with greater rightward asymmetry with age.<h4>Conclusions</h4>results provide evidence for rightward asymmetry in auditory association areas (pSTG and PT) known to subserve language processing. Cumulatively, our data provide evidence for a differing maturational path for PT for lower functioning children with AD, with both pre- and post-natal experience likely playing a role in PT asymmetry.<h4>Electronic supplementary material</h4>The online version of this article (doi:10.1007/s11689-009-9010-2) contains supplementary material, which is available to authorized users.
Project description:Brain plasticity has often been quoted as a reason for the more favorable outcome in childhood stroke compared to adult stroke. We investigated the relationship between language abilities and language localization in childhood stroke. Seventeen children and adolescents with left- or right-sided ischemic stroke and 18 healthy controls were tested with a comprehensive neurolinguistic test battery, and the individual neural representation of language was measured with an fMRI language paradigm. Overall, 12 of 17 stroke patients showed language abilities below average, and five patients exhibited impaired language performance. fMRI revealed increased activity in right hemisphere areas homotopic to left hemisphere language regions. In sum, seven stroke patients revealed atypical, i.e. bilateral or right lateralized language representation. Typical left hemispheric language lateralization was associated with better performance in naming and word fluency, whereas increased involvement of right homologues was accompanied by worse language outcome. In contrast, lesion lateralization or lesion volume did not correlate with language outcome or atypical language lateralization. Thus, atypical language lateralization is unfavorable for language outcome, and right homologues do not have the same cognitive capacity, even in young children.
Project description:This study combines functional and structural magnetic resonance imaging to test the "asymmetric sampling in time" (AST) hypothesis, which makes assertions about the symmetrical and asymmetrical representation of speech in the primary and nonprimary auditory cortex. Twenty-three volunteers participated in this parametric clustered-sparse fMRI study. The availability of slowly changing acoustic cues in spoken sentences was systematically reduced over continuous segments with varying lengths (100, 150, 200, 250 ms) by utilizing local time-reversion. As predicted by the hypothesis, functional lateralization in Heschl's gyrus could not be observed. Lateralization in the planum temporale and posterior superior temporal gyrus shifted towards the right hemisphere with decreasing suprasegmental temporal integrity. Cortical thickness of the planum temporale was automatically measured. Participants with an L > R cortical thickness performed better on the in-scanner auditory pattern-matching task. Taken together, these findings support the AST hypothesis and provide substantial novel insight into the division of labor between left and right nonprimary auditory cortex functions during comprehension of spoken utterances. In addition, the present data yield support for a structural-behavioral relationship in the nonprimary auditory cortex.
Project description:One prominent theory in neuroscience and psychology assumes that cortical regions for language are left hemisphere lateralized in the human brain. In the current study, we used a novel technique, quantitative magnetic resonance imaging (qMRI), to examine interhemispheric asymmetries in language regions in terms of macromolecular tissue volume (MTV) and quantitative longitudinal relaxation time (T1) maps in the living human brain. These two measures are known to reflect cortical myeloarchitecture from the microstructural perspective. One hundred and fifteen adults (55 male, 60 female) were examined for their myeloarchitectonic asymmetries of language regions. We found that the cortical myeloarchitecture of inferior frontal areas including the pars opercularis, pars triangularis, and pars orbitalis is left lateralized, while that of the middle temporal gyrus, Heschl's gyrus, and planum temporale is right lateralized. Moreover, the leftward lateralization of myelination structure is significantly correlated with language skills measured by phonemic and speech tone awareness. This study reveals for the first time a mixed pattern of myeloarchitectonic asymmetries, which calls for a general theory to accommodate the full complexity of principles underlying human hemispheric specialization.
Project description:The current study investigated behavioral correlates of structural asymmetry of the insula, and traditional perisylvian language regions, in a large sample of young adults (N=200). The findings indicated (1) reliable leftward surface area asymmetry of the anterior insula, (2) association of this asymmetry with divided visual field lateralization of visual word recognition, and (3) modulation of the correlation of structural and linguistic asymmetry by consistency of hand preference. Although leftward asymmetry of cortical surface area was observed for the anterior insula, pars opercularis and triangularis, and planum temporale, only the anterior insula asymmetry was associated with lateralized word recognition. We interpret these findings within the context of recent structural and functional findings about the human insula. We suggest that leftward structural lateralization of earlier developing insular cortex may bootstrap asymmetrical functional lateralization even if the insula is only a minor component of the adult language network.
Project description:Hemispheric lateralization for language production and its relationships with manual preference and manual preference strength were studied in a sample of 297 subjects, including 153 left-handers (LH). A hemispheric functional lateralization index (HFLI) for language was derived from fMRI acquired during a covert sentence generation task as compared with a covert word list recitation. The multimodal HFLI distribution was optimally modeled using a mixture of 3 and 4 Gaussian functions in right-handers (RH) and LH, respectively. Gaussian function parameters helped to define 3 types of language hemispheric lateralization, namely "Typical" (left hemisphere dominance with clear positive HFLI values, 88% of RH, 78% of LH), "Ambilateral" (no dominant hemisphere with HFLI values close to 0, 12% of RH, 15% of LH) and "Strongly-atypical" (right-hemisphere dominance with clear negative HFLI values, 7% of LH). Concordance between dominant hemispheres for hand and for language did not exceed chance level, and most of the association between handedness and language lateralization was explained by the fact that all Strongly-atypical individuals were left-handed. Similarly, most of the relationship between language lateralization and manual preference strength was explained by the fact that Strongly-atypical individuals exhibited a strong preference for their left hand. These results indicate that concordance of hemispheric dominance for hand and for language occurs barely above the chance level, except in a group of rare individuals (less than 1% in the general population) who exhibit strong right hemisphere dominance for both language and their preferred hand. They call for a revisit of models hypothesizing common determinants for handedness and for language dominance.
Project description:Human language is dominantly processed in the left cerebral hemisphere in most of the population. While several studies have suggested that there are higher rates of atypical right-hemispheric language lateralization in left-/mixed-handers, an accurate estimate of this association from a large sample is still missing. In this study, we comprised data from 1,554 individuals sampled in three previous studies in which language lateralization measured via dichotic listening, handedness and footedness were assessed. Overall, we found a right ear advantage indicating typical left-hemispheric language lateralization in 82.1% of the participants. While we found significantly more left-handed individuals with atypical language lateralization on the categorical level, we only detected a very weak positive correlation between dichotic listening lateralization quotients (LQs) and handedness LQs using continuous measures. Here, only 0.4% of the variance in language lateralization were explained by handedness. We complemented these analyses with Bayesian statistics and found no evidence in favor of the hypothesis that language lateralization and handedness are related. Footedness LQs were not correlated with dichotic listening LQs, but individuals with atypical language lateralization also exhibited higher rates of atypical footedness on the categorical level. We also found differences in the extent of language lateralization between males and females with males exhibiting higher dichotic listening LQs indicating more left-hemispheric language processing. Overall, these findings indicate that the direct associations between language lateralization and motor asymmetries are much weaker than previously assumed with Bayesian correlation analyses even suggesting that they do not exist at all. Furthermore, sex differences seem to be present in language lateralization when the power of the study is adequate suggesting that endocrinological processes might influence this phenotype.