Microstructural Properties of the Cerebellar Peduncles in Children With Developmental Language Disorder.

Children with developmental language disorder (DLD) struggle to learn their native language for no apparent reason. While research on the neurobiological underpinnings of the disorder has focused on the role of corticostriatal systems, little is known about the role of the cerebellum in DLD. Corticocerebellar circuits might be involved in the disorder as they contribute to complex sensorimotor skill learning, including the acquisition of spoken language. Here, we used diffusion-weighted imaging data from 77 typically developing and 54 children with DLD and performed probabilistic tractography to identify the cerebellum's white matter tracts: the inferior, middle, and superior cerebellar peduncles. Children with DLD showed lower fractional anisotropy (FA) in the inferior cerebellar peduncles (ICP), fiber tracts that carry motor and sensory input via the inferior olive to the cerebellum. Lower FA in DLD was driven by lower axial diffusivity. Probing this further with more sophisticated modeling of diffusion data, we found higher orientation dispersion but no difference in neurite density in the ICP of children with DLD. Reduced FA is therefore unlikely to be reflecting microstructural differences in myelination, rather the organization of axons in these pathways is disrupted. ICP microstructure was not associated with language or motor coordination performance in our sample. We also found no differences in the middle and superior peduncles, the main pathways connecting the cerebellum with the cortex. To conclude, it is not corticocerebellar but atypical olivocerebellar white matter connections that characterize DLD and suggest the involvement of the olivocerebellar system in speech and language acquisition and development.

Differences in Cortical Surface Area in Developmental Language Disorder.

Approximately 7% of children have developmental language disorder (DLD), a neurodevelopmental condition associated with persistent language learning difficulties without a known cause. Our understanding of the neurobiological basis of DLD is limited. Here, we used FreeSurfer to investigate cortical surface area and thickness in a large cohort of 156 children and adolescents aged 10-16 years with a range of language abilities, including 54 with DLD, 28 with a history of speech-language difficulties who did not meet criteria for DLD, and 74 age-matched controls with typical language development (TD). We also examined cortical asymmetries in DLD using an automated surface-based technique. Relative to the TD group, those with DLD showed smaller surface area bilaterally in the inferior frontal gyrus extending to the anterior insula, in the posterior temporal and ventral occipito-temporal cortex, and in portions of the anterior cingulate and superior frontal cortex. Analysis of the whole cohort using a language proficiency factor revealed that language ability correlated positively with surface area in similar regions. There were no differences in cortical thickness, nor in asymmetry of these cortical metrics between TD and DLD. This study highlights the importance of distinguishing between surface area and cortical thickness in investigating the brain basis of neurodevelopmental disorders and suggests the development of cortical surface area to be of importance to DLD. Future longitudinal studies are required to understand the developmental trajectory of these cortical differences in DLD and how they relate to language maturation.

Microstructural Properties of the Cerebellar Peduncles in Children with Developmental Language Disorder.

Children with developmental language disorder (DLD) struggle to learn their native language for no apparent reason. While research on the neurobiological underpinnings of the disorder has focused on the role of cortico-striatal systems, little is known about the role of the cerebellum in DLD. Cortico-cerebellar circuits might be involved in the disorder as they contribute to complex sensorimotor skill learning, including the acquisition of spoken language. Here, we used diffusion-weighted imaging data from 77 typically developing and 54 children with DLD and performed probabilistic tractography to identify the cerebellum's white matter tracts: the inferior, middle, and superior cerebellar peduncles. Children with DLD showed lower fractional anisotropy (FA) in the inferior cerebellar peduncles (ICP), fiber tracts that carry motor and sensory input via the inferior olive to the cerebellum. Lower FA in DLD was driven by lower axial diffusivity. Probing this further with more sophisticated modeling of diffusion data, we found higher orientation dispersion but no difference in neurite density in the ICP of DLD. Reduced FA is therefore unlikely to be reflecting microstructural differences in myelination in this tract, rather the organization of axons in these pathways is disrupted. ICP microstructure was not associated with language or motor coordination performance in our sample. We also found no differences in the middle and superior peduncles, the main pathways connecting the cerebellum with the cortex. To conclude, it is not cortico-cerebellar but atypical olivocerebellar white matter connections that characterize DLD and suggest the involvement of the olivocerebellar system in speech acquisition and development.

Quantitative MRI reveals differences in striatal myelin in children with DLD.

Developmental language disorder (DLD) is a common neurodevelopmental disorder characterised by receptive or expressive language difficulties or both. While theoretical frameworks and empirical studies support the idea that there may be neural correlates of DLD in frontostriatal loops, findings are inconsistent across studies. Here, we use a novel semiquantitative imaging protocol - multi-parameter mapping (MPM) - to investigate microstructural neural differences in children with DLD. The MPM protocol allows us to reproducibly map specific indices of tissue microstructure. In 56 typically developing children and 33 children with DLD, we derived maps of (1) longitudinal relaxation rate R1 (1/T1), (2) transverse relaxation rate R2* (1/T2*), and (3) Magnetization Transfer saturation (MTsat). R1 and MTsat predominantly index myelin, while R2* is sensitive to iron content. Children with DLD showed reductions in MTsat values in the caudate nucleus bilaterally, as well as in the left ventral sensorimotor cortex and Heschl's gyrus. They also had globally lower R1 values. No group differences were noted in R2* maps. Differences in MTsat and R1 were coincident in the caudate nucleus bilaterally. These findings support our hypothesis of corticostriatal abnormalities in DLD and indicate abnormal levels of myelin in the dorsal striatum in children with DLD.

Seven percent of children struggle to learn their native language for no obvious reason. This condition is called Developmental Language Disorder (DLD). Children with DLD often have difficulty learning to read and write. They are at higher risk for academic underachievement and may struggle to find good jobs. Their language difficulties also contribute to difficulties making friends and emotional challenges. Scientists suspect children with DLD may have differences in areas deep in the brain that help people learn habits and rules. A new magnetic resonance imaging technique called multiparameter mapping (MPM) can help scientists determine if this is true. The technique measures the properties of brain tissue. It is particularly useful for measuring the amounts of a fatty protective sheath on brain cells called myelin. Myelin helps brain cells send information faster. Using MPM, Krishnan et al. show that children with DLD have less myelin in parts of the brain responsible for speaking, listening, and learning rules and habits. In the experiments, 56 children with typical language development and 33 children with DLD were scanned using MPM. Krishnan et al. then compared the two groups and found reduced myelin in these critical areas associated with learning a language in most of the children with DLD. But not all children with DLD had these differences. More studies are needed to determine if these brain differences cause language problems and how or if experiencing language difficulties could cause these changes in the brain. Further research may help scientists find new treatments that target these brain differences.

Parent Language Input Prior to School Forecasts Change in Children's Language-Related Cortical Structures During Mid-Adolescence.

Children differ widely in their early language development, and this variability has important implications for later life outcomes. Parent language input is a strong experiential factor predicting the variability in children's early language skills. However, little is known about the brain or cognitive mechanisms that underlie the relationship. In addressing this gap, we used longitudinal data spanning 15 years to examine the role of early parental language input that children receive during preschool years in the development of brain structures that support language processing during school years. Using naturalistic parent-child interactions, we measured parental language input (amount and complexity) to children between the ages of 18 and 42 months (n = 23). We then assessed longitudinal changes in children's cortical thickness measured at five time points between 9 and 16 years of age. We focused on specific regions of interest (ROIs) that have been shown to play a role in language processing. Our results support the view that, even after accounting for important covariates such as parental intelligence quotient (IQ) and education, the amount and complexity of language input to a young child prior to school forecasts the rate of change in cortical thickness during the 7-year period from 5½ to 12½ years later. Examining the proximal correlates of change in brain and cognitive differences has the potential to inform targets for effective prevention and intervention strategies.

Functional organisation for verb generation in children with developmental language disorder.

Developmental language disorder (DLD) is characterised by difficulties in learning one's native language for no apparent reason. These language difficulties occur in 7% of children and are known to limit future academic and social achievement. Our understanding of the brain abnormalities associated with DLD is limited. Here, we used a simple four-minute verb generation task (children saw a picture of an object and were instructed to say an action that goes with that object) to test children between the ages of 10-15 years (DLD N = 50, typically developing N = 67). We also tested 26 children with poor language ability who did not meet our criteria for DLD. Contrary to our registered predictions, we found that children with DLD did not have (i) reduced activity in language relevant regions such as the left inferior frontal cortex; (ii) dysfunctional striatal activity during overt production; or (iii) a reduction in left-lateralised activity in frontal cortex. Indeed, performance of this simple language task evoked activity in children with DLD in the same regions and to a similar level as in typically developing children. Consistent with previous reports, we found sub-threshold group differences in the left inferior frontal gyrus and caudate nuclei, but only when analysis was limited to a subsample of the DLD group (N = 14) who had the poorest performance on the task. Additionally, we used a two-factor model to capture variation in all children studied (N = 143) on a range of neuropsychological tests and found that these language and verbal memory factors correlated with activity in different brain regions. Our findings indicate a lack of support for some neurological models of atypical language learning, such as the procedural deficit hypothesis or the atypical lateralization hypothesis, at least when using simple language tasks that children can perform. These results also emphasise the importance of controlling for and monitoring task performance.

Asymmetry of Auditory-Motor Speech Processing is Determined by Language Experience.

Speech processing relies on interactions between auditory and motor systems and is asymmetrically organized in the human brain. The left auditory system is specialized for processing of phonemes, whereas the right is specialized for processing of pitch changes in speech affecting prosody. In speakers of tonal languages, however, processing of pitch (i.e., tone) changes that alter word meaning is left-lateralized indicating that linguistic function and language experience shape speech processing asymmetries. Here, we investigated the asymmetry of motor contributions to auditory speech processing in male and female speakers of tonal and non-tonal languages. We temporarily disrupted the right or left speech motor cortex using transcranial magnetic stimulation (TMS) and measured the impact of these disruptions on auditory discrimination (mismatch negativity; MMN) responses to phoneme and tone changes in sequences of syllables using electroencephalography (EEG). We found that the effect of motor disruptions on processing of tone changes differed between language groups: disruption of the right speech motor cortex suppressed responses to tone changes in non-tonal language speakers, whereas disruption of the left speech motor cortex suppressed responses to tone changes in tonal language speakers. In non-tonal language speakers, the effects of disruption of left speech motor cortex on responses to tone changes were inconclusive. For phoneme changes, disruption of left but not right speech motor cortex suppressed responses in both language groups. We conclude that the contributions of the right and left speech motor cortex to auditory speech processing are determined by the functional roles of acoustic cues in the listener's native language.SIGNIFICANCE STATEMENT The principles underlying hemispheric asymmetries of auditory speech processing remain debated. The asymmetry of processing of speech sounds is affected by low-level acoustic cues, but also by their linguistic function. By combining transcranial magnetic stimulation (TMS) and electroencephalography (EEG), we investigated the asymmetry of motor contributions to auditory speech processing in tonal and non-tonal language speakers. We provide causal evidence that the functional role of the acoustic cues in the listener's native language affects the asymmetry of motor influences on auditory speech discrimination ability [indexed by mismatch negativity (MMN) responses]. Lateralized top-down motor influences can affect asymmetry of speech processing in the auditory system.

Language development and brain reorganization in a child born without the left hemisphere.

We present a case of a 14-year-old girl born without the left hemisphere due to prenatal left internal carotid occlusion. We combined longitudinal language and cognitive assessments with functional and structural neuroimaging data to situate the case within age-matched, typically developing children. Despite having had a delay in getting language off the ground during the preschool years, our case performed within the normal range on a variety of standardized language tests, and exceptionally well on phonology and word reading, during the elementary and middle school years. Moreover, her spatial, number, and reasoning skills also fell in the average to above-average range based on assessments during these time periods. Functional MRI data revealed activation in right fronto-temporal areas when listening to short stories, resembling the bilateral activation patterns in age-matched typically developing children. Diffusion MRI data showed significantly larger dorsal white matter association tracts (the direct and anterior segments of the arcuate fasciculus) connecting areas active during language processing in her remaining right hemisphere, compared to either hemisphere in control children. We hypothesize that these changes in functional and structural brain organization are the result of compensatory brain plasticity, manifesting in unusually large right dorsal tracts, and exceptional performance in phonology, speech repetition, and decoding. More specifically, we posit that our case's large white matter connections might have played a compensatory role by providing fast and reliable transfer of information between cortical areas for language in the right hemisphere.

Functional neuroanatomy of gesture-speech integration in children varies with individual differences in gesture processing.

Gesture is an integral part of children's communicative repertoire. However, little is known about the neurobiology of speech and gesture integration in the developing brain. We investigated how 8- to 10-year-old children processed gesture that was essential to understanding a set of narratives. We asked whether the functional neuroanatomy of gesture-speech integration varies as a function of (1) the content of speech, and/or (2) individual differences in how gesture is processed. When gestures provided missing information not present in the speech (i.e., disambiguating gesture; e.g., "pet" + flapping palms = bird), the presence of gesture led to increased activity in inferior frontal gyri, the right middle temporal gyrus, and the left superior temporal gyrus, compared to when gesture provided redundant information (i.e., reinforcing gesture; e.g., "bird" + flapping palms = bird). This pattern of activation was found only in children who were able to successfully integrate gesture and speech behaviorally, as indicated by their performance on post-test story comprehension questions. Children who did not glean meaning from gesture did not show differential activation across the two conditions. Our results suggest that the brain activation pattern for gesture-speech integration in children overlaps with-but is broader than-the pattern in adults performing the same task. Overall, our results provide a possible neurobiological mechanism that could underlie children's increasing ability to integrate gesture and speech over childhood, and account for individual differences in that integration.

The pace of vocabulary growth during preschool predicts cortical structure at school age.

Children vary greatly in their vocabulary development during preschool years. Importantly, the pace of this early vocabulary growth predicts vocabulary size at school entrance. Despite its importance for later academic success, not much is known about the relation between individual differences in early vocabulary development and later brain structure and function. Here we examined the association between vocabulary growth in children, as estimated from longitudinal measurements from 14 to 58 months, and individual differences in brain structure measured in 3rd and 4th grade (8-10 years old). Our results show that the pace of vocabulary growth uniquely predicts cortical thickness in the left supramarginal gyrus. Probabilistic tractography revealed that this region is directly connected to the inferior frontal gyrus (pars opercularis) and the ventral premotor cortex, via what is most probably the superior longitudinal fasciculus III. Our findings demonstrate, for the first time, the relation between the pace of vocabulary learning in children and a specific change in the structure of the cerebral cortex, specifically, cortical thickness in the left supramarginal gyrus. They also highlight the fact that differences in the pace of vocabulary growth are associated with the dorsal language stream, which is thought to support speech perception and articulation.

Repetition Suppression in the Left Inferior Frontal Gyrus Predicts Tone Learning Performance.

Do individuals differ in how efficiently they process non-native sounds? To what extent do these differences relate to individual variability in sound-learning aptitude? We addressed these questions by assessing the sound-learning abilities of Dutch native speakers as they were trained on non-native tone contrasts. We used fMRI repetition suppression to the non-native tones to measure participants' neuronal processing efficiency before and after training. Although all participants improved in tone identification with training, there was large individual variability in learning performance. A repetition suppression effect to tone was found in the bilateral inferior frontal gyri (IFGs) before training. No whole-brain effect was found after training; a region-of-interest analysis, however, showed that, after training, repetition suppression to tone in the left IFG correlated positively with learning. That is, individuals who were better in learning the non-native tones showed larger repetition suppression in this area. Crucially, this was true even before training. These findings add to existing evidence that the left IFG plays an important role in sound learning and indicate that individual differences in learning aptitude stem from differences in the neuronal efficiency with which non-native sounds are processed.

Effects of Early Bilingual Experience with a Tone and a Non-Tone Language on Speech-Music Integration.

We investigated music and language processing in a group of early bilinguals who spoke a tone language and a non-tone language (Cantonese and Dutch). We assessed online speech-music processing interactions, that is, interactions that occur when speech and music are processed simultaneously in songs, with a speeded classification task. In this task, participants judged sung pseudowords either musically (based on the direction of the musical interval) or phonologically (based on the identity of the sung vowel). We also assessed longer-term effects of linguistic experience on musical ability, that is, the influence of extensive prior experience with language when processing music. These effects were assessed with a task in which participants had to learn to identify musical intervals and with four pitch-perception tasks. Our hypothesis was that due to their experience in two different languages using lexical versus intonational tone, the early Cantonese-Dutch bilinguals would outperform the Dutch control participants. In online processing, the Cantonese-Dutch bilinguals processed speech and music more holistically than controls. This effect seems to be driven by experience with a tone language, in which integration of segmental and pitch information is fundamental. Regarding longer-term effects of linguistic experience, we found no evidence for a bilingual advantage in either the music-interval learning task or the pitch-perception tasks. Together, these results suggest that being a Cantonese-Dutch bilingual does not have any measurable longer-term effects on pitch and music processing, but does have consequences for how speech and music are processed jointly.

Speech and music shape the listening brain: evidence for shared domain-general mechanisms.

Are there bi-directional influences between speech perception and music perception? An answer to this question is essential for understanding the extent to which the speech and music that we hear are processed by domain-general auditory processes and/or by distinct neural auditory mechanisms. This review summarizes a large body of behavioral and neuroscientific findings which suggest that the musical experience of trained musicians does modulate speech processing, and a sparser set of data, largely on pitch processing, which suggest in addition that linguistic experience, in particular learning a tone language, modulates music processing. Although research has focused mostly on music on speech effects, we argue that both directions of influence need to be studied, and conclude that the picture which thus emerges is one of mutual interaction across domains. In particular, it is not simply that experience with spoken language has some effects on music perception, and vice versa, but that because of shared domain-general subcortical and cortical networks, experiences in both domains influence behavior in both domains.