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Journal ArticleDOI

A Brain Marker for Developmental Speech Disorders.

01 Jul 2018-The Journal of Pediatrics (Mosby)-Vol. 198

TL;DR: Atypical development of the left corticobulbar tract may be a neural marker for DSD, and changes for language disorders are likely more complex.

AbstractObjective To characterize the organization of speech- and language-related white matter tracts in children with developmental speech and/or language disorders. Study design We collected magnetic resonance diffusion-weighted imaging data from 41 children, ages 9-11 years, with developmental speech and/or language disorders, and compared them with 45 typically developing controls with the same age range. We used probabilistic tractography of diffusion-weighted imaging to map language (3 segments of arcuate fasciculus, extreme capsule system) and speech motor (corticobulbar) tracts bilaterally. The corticospinal and callosal tracts were used as control regions. We compared the mean fractional anisotropy and diffusivity values between atypical and control groups, covarying for nonverbal IQ. We then examined differences between atypical subgroups: developmental speech disorder (DSD), developmental language disorder, and co-occurring developmental speech and language disorder. Results Fractional anisotropy in the left corticobulbar tract was lower in the DSD than in the control group. Radial and mean diffusivity were higher in the DSD than the developmental language disorder, co-occurring developmental speech and language disorder, or control groups. There were no group differences for any metrics in the language or control tracts. Conclusions Atypical development of the left corticobulbar tract may be a neural marker for DSD. This finding is in line with reports of speech disorder after left corticobulbar damage in children and adults with brain injury. By contrast, we found no association between diffusion metrics in language-related tracts in developmental language disorder, and changes for language disorders are likely more complex.

Topics: Speech disorder (64%), Language disorder (64%), Tractography (53%), Arcuate fasciculus (50%)

Summary (2 min read)

INTRODUCTION

  • Developmental speech and language disorders are common, seen in 1 in 20 preschool children, in the absence of neurological deficits, intellectual impairment or hearing loss.
  • Most recently, diffusion weighted imaging and tractography have become promising tools as measures of white matter organization, allowing us to examine structural brain connectivity in these conditions.
  • The dorsal pathway matures at a later stage of development and has been suggested to be involved in more complex language functions.
  • Of note, the absence of such findings could be in part because existing studies include highly selected, cross-sectionally recruited, clinical samples (see 10-12 for review), with limited generalizability of findings to the broader DLD population.
  • The authors hypothesized developmental speech and language disorders would be associated with atypical development of speech-motor and language (dorsal and ventral streams) tracts, respectively.

Participant recruitment

  • Participants (N = 86, age range: 9.25-11.25 years) were recruited from the Early Language in Victoria Study (ELVS), a longitudinal community-based study of 1900 children.
  • Age of scanning was carefully chosen to reflect a time when communication trajectories are relatively stable.
  • Some attrition occurred across the 4 and 5 year old waves of the ELVS, hence expanding the DLD inclusion criteria across 2 data waves provided a larger pool for recruitment.
  • Articulation disorder could also include an omission error where the phone was absent in the child’s inventory, but it appears in the phonetic inventory of >90% of peers in normative data.22-24 Phonological delay was use of a phonological process that occurs in typically developing speech, but is used beyond an age where it is typically resolved in >90% of peers.
  • Exclusion criteria were a history of neurological, hearing, genetic or neurodevelopmental disorders (e.g., autistic spectrum disorder) and non-English speaking background.

Procedure

  • At the time of scanning, participants were assessed with the same speech, language and nonverbal IQ tests reported above for participant group selection (Table 1).
  • Standardized scores were used for the CELF-IV26 and WASI.19 Clinical diagnosis of DSD was made based on phonetic transcription and phonological process analysis.

Preprocessing of MRI datasets

  • DWI datasets were pre-processed using MRtrix.27 Fractional anisotropy (FA) and eigenvector maps were extracted.
  • Constrained spherical deconvolution was used to estimate the distribution of fiber orientations.
  • This is an optimal method relative to the diffusion tensor model, in areas with multiple crossing fibers.

Tractography

  • Conventional MRI scans were confirmed to be normal.
  • Tractography delineated all tracts in all participants, with the exception of 8 instances in which no streamlines were generated for the posterior segment of the AF (TD=4, DLD=1, DSD=3, DSLD=3).
  • Consistent with this finding, univariate analyses also revealed trends for a group difference and group by hemisphere effect for the CBT only.
  • Post-hoc tests showed that FA in the left CBT was significantly different between DSD and TD groups only (Bonferroni corrected p=.045).

Clinical presentation

  • The 4 groups were matched for demographic characteristics (Table 1).
  • Non-verbal IQ scores, although within the typical range, were lower in DLD children than in children with DSD as commonly reported in this group.
  • Children with DSLD had a more phonological presentation at age 4 but by age 9-11, at time of scanning, the majority of this group also had articulation errors.
  • Slightly more participants in the DSD (72%) than DSLD (64%) group had articulation errors at time of scanning.

DISCUSSION

  • The authors report the first association between developmental speech disorder and reduced FA of the left corticobulbar tract, suggesting atypical development of this tract may be a neural marker for DSD.
  • Altered connectivity of the left CBT has previously been associated with speech disorder in different childhood populations and disease models including childhood stuttering14 and dysarthria after childhood traumatic brain injury.
  • 10-12 Methodological approaches unique to this study represented important methodological strengths in the study of potential neural markers.
  • These included longitudinally-informed selection of participants from a community cohort, within a narrow age range, and co-varying for NVIQ.

AUTHOR CONTRIBUTIONS

  • AM, FL, SR, AC, GCR designed the research, supervised the data collection.
  • AM, FL, MS, AC, SR, GCR performed the research.
  • MS, FL analyzed and interpreted the MRI data.
  • AM, FL, LP, MS, SR, GCR analysed and interpreted the behavioural data.
  • All authors contributed to writing and revision of the final manuscript.

ACKNOWLEDGMENTS

  • The authors thank all participants and their families for their time and support.
  • The authors also thank J.-D.T. for helpful input regarding MRTrix, Lauren Pigdon (Murdoch Children’s Research Institute, Melbourne; nil relevant funding sources and nil conflicts of interest) for data collection and Shawna Farquharson (Florey Institute of Neuroscience and Mental Health Melbourne; nil relevant funding sources and nil conflicts of interest) and her team of radiographers for scanning participants.
  • AM, SR, and AC are grateful to the Operational Infrastructure Support Program of the State Government of Victoria for their support.

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1
A brain marker for developmental speech disorder
Short title: A brain marker for developmental speech disorder
Angela T. Morgan*
1,2
, Merina Su
3
, Sheena Reilly
1,4
, Gina Conti-Ramsden
5
, Alan Connelly,
6
Frédérique J. Liégeois
3
Affiliations
1. Murdoch Children's Research Institute and Royal Children's Hospital, Melbourne, Australia
2. University of Melbourne, Australia
3. UCL Great Ormond Street Institute of Child Health, London, UK
4. Griffith University, Gold Coast, Australia
5. School of Health Sciences, The University of Manchester, UK
6. Florey Institute of Neuroscience and Mental Health, Melbourne, Australia
Corresponding author:
Angela Morgan
Neuroscience of Speech, Murdoch Children’s Research Institute, Royal Children’s Hospital
Melbourne, Australia. E-mail: angela.morgan@mcri.edu.au; Ph: +61 406 971 454.
Word count: 2272
STUDY FUNDING
This study was supported by National Health and Medical Research Council (NHMRC)
Centre of Research Excellence (CRE) grant (1023493) awarded to SR, AM and AC;
NHMRC CRE (1116976) awarded to AM, AC, SR; NHMRC Career Development
Fellowship (607315) and NHMRC Practitioner Fellowship (1105008) awarded to AM;
Hearing CRC grant awarded to SR, AM. The authors report no disclosures relevant to the
manuscript. Go to Neurology.org for full disclosures.

2
ABSTRACT
Objective: To characterise the organisation of speech- and language-related white matter
tracts in children with developmental speech and/or language disorders.
Study design: We collected Diffusion Weighted Imaging (DWI) data from 86 children aged
9 to 11 years, with developmental speech and/or language disorders (N=41) and typically
developing controls (TD, N=45). We used probabilistic tractography of DWI to map
language (3 segments of arcuate fasciculus, extreme capsule system) and speech motor
(corticobulbar) tracts, bilaterally. The corticospinal and callosal tracts were used as control
regions. We compared mean fractional anisotropy (FA) and diffusivity values between
atypical and TD groups, co-varying for non-verbal IQ. We then examined differences
between atypical sub-groups; developmental speech disorder (DSD), developmental language
disorder (DLD), and co-occurring developmental speech and language disorder (DSLD).
Results: FA in the left corticobulbar tract was lower in the DSD than in the TD group. Radial
and mean diffusivity were higher in the DSD than the DLD, DSLD or TD groups. There were
no group differences for any metrics in the language or control tracts.
Conclusions: Atypical development of the left corticobulbar tract may be a neural marker for
DSD. This finding is in line with reports of speech disorder following left corticobulbar damage
in children and adults with brain injury. By contrast, we found no association between diffusion
metrics in language-related tracts in DLD. Early white matter disruption in DLD may be
heterogeneous across cases, in line with the incongruent findings of past MRI studies in the
field, and the phenotypic heterogeneity characteristic of this group.
Key words: child; diffusion weighted imaging; tractography; arcuate fasciculus; corticobulbar

3
INTRODUCTION
Developmental speech and language disorders are common, seen in 1 in 20 preschool
children, in the absence of neurological deficits, intellectual impairment or hearing loss.
1-4
These conditions are a leading cause of children presenting to General Practitioners and
paediatricians. Developmental speech disorders (DSD; affecting how clearly speech sounds
are produced) and language disorders (DLD; affecting language structure such as grammar
and semantics) often co-occur, but also dissociate. DLD was previously known as specific
language impairment, but international consensus has agreed on DLD nomenclature.
2
Despite
100 years of phenotypic investigation, no reliable symptom-based prognostic markers exist.
Hence interest has intensified in examining MR-based neural markers. Most recently,
diffusion weighted imaging and tractography have become promising tools as measures of
white matter organization, allowing us to examine structural brain connectivity in these
conditions.
A ventral (extreme capsule system) and dorsal route (arcuate fasciculus) have been
implicated in typical child language development, with a ‘maturational primacy’ in the
ventral route, present at birth.
5,6
The dorsal pathway matures at a later stage of development
and has been suggested to be involved in more complex language functions.
5
Few studies,
however, have reported reductions in fractional anisotropy (FA) and radial diffusivity (RD)
metrics of either stream of this ‘traditional language tract’ in children with DLD.
7-9
Of note,
the absence of such findings could be in part because existing studies include highly selected,
cross-sectionally recruited, clinical samples (see
10-12
for review), with limited
generalizability of findings to the broader DLD population. Current studies also fail to
examine ‘control’ tracts outside hypothesized language regions, obscuring whether findings
are localized to language-tracts or widespread throughout the brain.

4
White matter integrity has not been examined in DSD to date, yet left corticobulbar tract
deficits have been reported in childhood dysarthria after brain injury
13
, childhood stuttering
14
,
adult dysarthria
15
and even in an adult case of neurodegenerative speech disorder in the
absence of language disorder.
16
Further, in relation to the developing system, no study has
directly compared white matter integrity of speech and language disordered groups together,
limiting knowledge of shared or distinct neural underpinnings.
Here we examined white matter connectivity in children with DLD, DSD and typically
developing controls. Participants were recruited from a longitudinal community cohort study
of speech and language. We hypothesized developmental speech and language disorders
would be associated with atypical development of speech-motor (corticobulbar) and language
(dorsal and ventral streams) tracts, respectively.
METHODS
Participant recruitment
Participants (N = 86, age range: 9.25-11.25 years) were recruited from the Early Language in
Victoria Study (ELVS), a longitudinal community-based study of 1900 children.
3
Communication status was collected almost annually from 8- 10 months of age
3
up to the age
of the current study (i.e., 9 to 11 years). Age of scanning was carefully chosen to reflect a
time when communication trajectories are relatively stable.
17
Ethical approval was granted by
the Royal Children’s Hospital Human Research Ethics Committee (Reference number
HREC31225).
Participants were recruited to 4 groups based on longitudinal data: Typically developing
controls (TD, n=45); Developmental Language Disorder (DLD, n=13); Developmental

5
Speech disorder (DSD, n=17); and co-occurring Developmental Speech and Language
disorders (DSLD, n=11). The three latter groups were combined into an “atypical” group for
the first stage of analyses; followed by sub-group analyses.
Inclusion criteria for all 4 groups included non-verbal IQ ≥ 80 on the Kaufman Brief
Intelligence Test
18
administered at age 4 and the Wechsler Abbreviated Scales of Intelligence
(WASI-II)
19
at age 7. DLD and TD groups were required to have typical speech as assessed
via the Goldman Fristoe Test of Articulation 2
nd
Edition (GFTA-II)
20
at ages 4 and 7. The
DLD group was also required to have impaired language, defined as a total language score of
≤ 81 (1.25 SD below the mean)
3
on the CELF-IV at two time points between at ages 4 and 7,
or 5 and 7. Some attrition occurred across the 4 and 5 year old waves of the ELVS, hence
expanding the DLD inclusion criteria across 2 data waves provided a larger pool for
recruitment. In contrast, children with DSD had articulation or phonological speech errors
consistent with DSD at ages 4 and 7.
21
To assess speech performance, the Goldman-Fristoe
Test of Articulation; GFTA-II (Goldman and Fristoe, 2005) was administered as a single-
word test that elicits all the speech sounds of English in initial, medial and final positions. All
sounds were transcribed and assessed for the presence of articulation and phonological errors
to confirm a diagnosis of DSD.
21,22
Articulation disorder was denoted as phonetic-based
distortions (e.g., lisps, de-rhoticism) where occurrence of the distortion was more frequent
than correct production of that phone. Articulation disorder could also include an omission
error where the phone was absent in the child’s inventory, but it appears in the phonetic
inventory of >90% of peers in normative data.
22-24
Phonological delay was use of a
phonological process that occurs in typically developing speech, but is used beyond an age
where it is typically resolved in >90% of peers.
23
Phonological disorder was use of a
phonological process that is atypical and seen in <10% the normative sample population at

Citations
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Journal ArticleDOI
TL;DR: A process-oriented approach to diagnosis and treatment planning of developmental speech disorders holds important advantages, offering direct leads for treatment aimed at the underlying impairment, tailored to the specific needs of the individual and adjusted to the developmental trajectory.
Abstract: Background Differential diagnosis and treatment planning of developmental speech disorders (DSD) remains a major challenge in paediatric speech-language pathology. Different classification systems exist, in which subtypes are differentiated based on their theoretical cause and in which the definitions generally refer to speech production processes. Accordingly, various intervention methods have been developed aiming at different parts of the speech production process. Diagnostic classification in these systems, however, is primarily based on a description of behavioural speech symptoms rather than on underlying deficits. Purpose In this paper, we present a process-oriented approach to diagnosis and treatment planning of DSD. Our framework comprises two general diagnostic categories: developmental delay and developmental disorder. Within these categories, treatment goals/targets and treatment methods are formulated at the level of processes and rules/representations. Conclusion A process-oriented approach to diagnosis and treatment planning holds important advantages, offering direct leads for treatment aimed at the underlying impairment, tailored to the specific needs of the individual and adjusted to the developmental trajectory.

25 citations


Journal ArticleDOI
TL;DR: Language, literacy and social-pragmatic deficits are common in males with Klinefelter syndrome, and data suggested a trend for more notable deficits with age and increasing academic and social demands.
Abstract: Background Speech and language deficits are frequent in males with Klinefelter syndrome (KS), yet the research base is slim and specific strengths and deficits in communication have not been well characterised. Nor have studies examined communication abilities across a wide age-range from infancy to adolescence. Objective To characterise communication in children and adolescents with KS. Method Twenty-six males, aged 1;1–17;4 years, took part in the study. Oromotor, speech, language, literacy and pragmatic abilities were assessed. Results Communication impairment was seen in 92% of cases (24/26), with salient findings being impairments in social-pragmatic language (15/18; 83%), language-memory (12/15; 80%) and literacy (13/17; 76%). Mild to severe receptive and expressive language deficits were common (16/23; 70%), although performance was varied across linguistic domains of semantics, syntax, and morphology. Oromotor impairment (21/21; 100%) and speech impairments were evident from preschool through to adolescence. Whilst speech was highly intelligible (22/26; 85%), articulation errors (12/26; 46%), phonological delay (12/26; 46%), phonological disorder (5/26; 19%) and dysarthria (2/23 8.7%) were observed. Other atypical, yet mild, speech features were noted such as hyponasality (16/23; 70%). Conclusions Language, literacy and social-pragmatic deficits are common in KS. Data suggested a trend for more notable deficits with age and increasing academic and social demands. We added novel data on the nature of speech production deficits, including persistent phonological errors in a number of cases. Earlier detection and intervention of phonological errors may reduce the risk for later language and literacy challenges and optimise academic, and ultimately social and behavioural difficulties later in life.

15 citations


Journal ArticleDOI
01 Apr 2019-Brain
TL;DR: Dorsal language stream is identified as a novel neural phenotype of developmental speech disorders, distinct from that reported in speech disorders associated with FOXP2 variants, and the data confirm the early role of this stream in auditory-to-articulation transformations.
Abstract: Speech disorders are highly prevalent in the preschool years, but frequently resolve. The neurobiological basis of the most persistent and severe form, apraxia of speech, remains elusive. Current neuroanatomical models of speech processing in adults propose two parallel streams. The dorsal stream is involved in sound to motor speech transformations, while the ventral stream supports sound/letter to meaning. Data-driven theories on the role of these streams during atypical speech and language development are lacking. Here we provide comprehensive behavioural and neuroimaging data on a large novel family where one parent and 11 children presented with features of childhood apraxia of speech (the same speech disorder associated with FOXP2 variants). The genetic cause of the disorder in this family remains to be identified. Importantly, in this family the speech disorder is not systematically associated with language or literacy impairment. Brain MRI scanning in seven children revealed large grey matter reductions over the left temporoparietal region, but not in the basal ganglia, relative to typically-developing matched peers. In addition, we detected white matter reductions in the arcuate fasciculus (dorsal language stream) bilaterally, but not in the inferior fronto-occipital fasciculus (ventral language stream) nor in primary motor pathways. Our findings identify disruption of the dorsal language stream as a novel neural phenotype of developmental speech disorders, distinct from that reported in speech disorders associated with FOXP2 variants. Overall, our data confirm the early role of this stream in auditory-to-articulation transformations. 10.1093/brain/awz018_video1 awz018media1 6018582401001.

14 citations


Journal ArticleDOI
TL;DR: Differences in language performance, white matter organization and structural lateralization of the language network were statistically analyzed and structural alterations might underlie the language impairment in children with DLD.
Abstract: This study aims to detect the neural substrate underlying the language impairment in children with developmental language disorder (DLD) using diffusion tensor imaging (DTI) tractography. Deterministic DTI tractography was performed in a group of right-handed children with DLD (N = 17; mean age 10;07 ± 2;01 years) and a typically developing control group matched for age, gender and handedness (N = 22; mean age 11;00 ± 1;11 years) to bilaterally identify the superior longitudinal fascicle, arcuate fascicle, anterior lateral segment and posterior lateral segment (also called dorsal language network) and the middle and inferior longitudinal fascicle, extreme capsule fiber system and uncinate fascicle (also called ventral language network). Language skills were assessed using an extensive, standardized test battery. Differences in language performance, white matter organization and structural lateralization of the language network were statistically analyzed. Children with DLD showed a higher overall volume and higher ADC values for the left-hemispheric language related WM tracts. In addition, in children with DLD, the majority (88%; 7/8) of the studied language related WM tracts did not show a significant left or right lateralization pattern. These structural alterations might underlie the language impairment in children with DLD.

10 citations


Journal ArticleDOI
TL;DR: The findings from this study suggest that this task is not a sensitive brain MRI marker for children with these disorders, unlike for individuals with single gene mutations like FOXP2 mutations.
Abstract: Developmental language disorder (DLD) and developmental speech disorder (DSD) are highly prevalent childhood conditions. An impaired ability to repeat nonsense words ("nonword repetition"), is claimed to be a robust behavioural marker for these conditions. Yet how brain function is altered during this task remains poorly understood. Previous research suggests that DLD or DSD may be associated with reduced brain activation in the inferior frontal and posterior temporal regions when compared to controls. However, this research is limited by within and between group variability in age, speech/language phenotype, and comorbidities. Here, we used functional MRI to examine brain activation during nonword repetition. As anticipated, behavioural findings confirmed that the DLD and DSD groups had poorer nonword repetition performance compared to typical controls. In contrast, fMRI revealed no statistically significant differences in brain activation, despite the groups appearing to engage slightly different regions when compared at identical thresholds. Therefore, whilst nonword repetition is a sensitive clinical marker for DLD and DSD, the findings from this study suggest that this task is not a sensitive brain MRI marker for children with these disorders, unlike for individuals with single gene mutations like FOXP2 mutations.

5 citations


Cites background from "A Brain Marker for Developmental Sp..."

  • ...Note that some participants in this study were also included in structural MRI focused publications (Kurth et al., 2018; Luders et al., 2017; Morgan et al., 2018)....

    [...]


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Q1. What contributions have the authors mentioned in the paper "A brain marker for developmental speech disorder short title: a brain marker for developmental speech disorder" ?

This paper examined white matter connectivity in children with DLD, DSD and typically developing controls, using diffusion weighted imaging and tractography to examine structural brain connectivity in these conditions.