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Brain Structure and Function

, Volume 224, Issue 9, pp 3387–3398 | Cite as

Grey matter volume in developmental speech and language disorder

  • Lauren Pigdon
  • Catherine Willmott
  • Sheena Reilly
  • Gina Conti-Ramsden
  • Christian Gaser
  • Alan Connelly
  • Angela T. MorganEmail author
Original Article

Abstract

Developmental language disorder (DLD) and developmental speech disorder (DSD) are common, yet their etiologies are not well understood. Atypical volume of the inferior and posterior language regions and striatum have been reported in DLD; however, variability in both methodology and study findings limits interpretations. Imaging research within DSD, on the other hand, is scarce. The present study compared grey matter volume in children with DLD, DSD, and typically developing speech and language. Compared to typically developing controls, children with DLD had larger volume in the right cerebellum, possibly associated with the procedural learning deficits that have been proposed in DLD. Children with DSD showed larger volume in the left inferior occipital lobe compared to controls, which may indicate a compensatory role of the visual processing regions due to sub-optimal auditory-perceptual processes. Overall, these findings suggest that different neural systems may be involved in the specific deficits related to DLD and DSD.

Keywords

Language Speech Child VBM MRI 

Notes

Acknowledgements

LP is funded by an Australian Government Research Training Program Stipend Scholarship. AM is supported by National Health and Medical Research Council Career (NHMRC) Development Fellowship #607315 and Practitioner Fellowship #1105008; NHMRC Centre of Research Excellence (CRE) in Child Language #1023493; NHMRC CRE Moving Ahead #1023043; and HEARing Collaborative Research Centre. This research is also supported by the CRE in Child Language #1023493 and the Victorian Government’s Operational Infrastructure Support Program. Thank you to Angela Mayes, Cristina Mei, and Sarah Barton for assistance with data collection.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Supplementary material

429_2019_1978_MOESM1_ESM.docx (202 kb)
Supplementary material 1 (DOCX 203 kb)

References

  1. Allen JS, Emmorey K, Bruss J, Damasio H (2013) Neuroanatomical differences in visual, motor, and language cortices between congenitally deaf signers, hearing signers, and hearing non-signers. Front Neuroanat 7:26.  https://doi.org/10.3389/fnana.2013.00026 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Badcock NA, Bishop DVM, Hardiman MJ, Barry JG, Watkins KE (2012) Co-localisation of abnormal brain structure and function in specific language impairment. Brain Lang 120:310–320.  https://doi.org/10.1016/j.bandl.2011.10.006 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Beal DS, Gracco VL, Brettschneider J, Kroll RM, De Nil LF (2013) A voxel-based morphometry (VBM) analysis of regional grey and white matter volume abnormalities within the speech production network of children who stutter. Cortex 49(8):2151–2161CrossRefGoogle Scholar
  4. Bergeson TR, Pisoni DB, Davis RAO (2005) Development of audiovisual comprehension skills in prelingually deaf children with cochlear implants. Ear Hear 26:149–164.  https://doi.org/10.1097/00003446-200504000- CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bishop DVM, Snowling MJ, Thompson PA, Greenhalgh T (2016) Catalise: a multinational and multidisciplinary Delphi consensus study. Identifying Lang Impairments child Pub Library Sci 11:e0158753.  https://doi.org/10.1371/journal.pone.0158753 CrossRefGoogle Scholar
  6. Campbell TF et al (2003) Risk factors for speech delay of unknown origin in 3-year-old children. Child Dev 74:346–357.  https://doi.org/10.1111/1467-8624.7402002 CrossRefPubMedGoogle Scholar
  7. Cho ZH (ed) (2015) 7.0 Telsla MRI brain atlas: in-vivo atlas with cryomacrotome correlation, 2nd edn. Springer, Heidelberg.  https://doi.org/10.1007/978-3-642-54398-2 Google Scholar
  8. Darby D, Walsh K (2005) Walsh’s neuropsychology: a clinical approach, 5th edn. Elsevier, EdinburghGoogle Scholar
  9. De Fossé L et al (2004) Language-association cortex asymmetry in autism and specific language impairment. Ann Neurol 56:757–766.  https://doi.org/10.1002/ana.20275 CrossRefPubMedGoogle Scholar
  10. Dodd B, Ttofari-Eecen K, Brommeyer K, Ng K, Reilly S, Morgan A (2018a) Delayed and disordered development of articulation and phonology between four and seven years. Child Lang Teach Therapy 34:87–99.  https://doi.org/10.1177/0265659017735958 CrossRefGoogle Scholar
  11. Dodd B, Reilly S, Ttofari-Eecen K, Morgan AT (2018b) Articulation or phonology? Evidence from longitudinal error data. Clin Linguist Phonet 32(11):1027–1041CrossRefGoogle Scholar
  12. Eadie P, Morgan AT, Ukoumunne OC, Ttofari Eecen K, Wake M, Reilly S (2015) Speech sound disorder at 4 years: Prevalence, comorbidities, and predictors in a community cohort of children. Dev Med Child Neurol 57:578–584.  https://doi.org/10.1111/dmcn.12635 CrossRefPubMedGoogle Scholar
  13. Edwards J, Fox RA, Rogers CL (2002) Final consonant discrimination in children: effects of phonological disorder, vocabulary size, and articulatory accuracy. J Speech Lang Hear Res 45:231–242.  https://doi.org/10.1092/4388/02/4502-0231 CrossRefPubMedGoogle Scholar
  14. Gauger LM, Lombardino LJ, Leonard CM (1997) Brain morphology in children with specific language impairment. J Speech Lang Hear Res 40:1272–1284CrossRefGoogle Scholar
  15. Girbau-Massana D, Garcia-Marti G, Marti-Bonmati L, Schwartz RG (2014) Gray-white matter and cerebrospinal fluid volume differences in children with specific language impairment and/or reading disability. Neuropsychologia 56:90–100.  https://doi.org/10.1016/j.neuropsychologia.2014.01.004 CrossRefPubMedGoogle Scholar
  16. Goldman R, Fristoe M (2000) The goldman-fristoe test of articulation, 2nd edn. American Guidance Service Inc, Circle PinesGoogle Scholar
  17. Graham SA, Fisher SE (2013) Decoding the genetics of speech and language. Curr Opin Neurobiol 23:43–51.  https://doi.org/10.1016/j.conb.2012.11.006 CrossRefPubMedGoogle Scholar
  18. Hayasaka S, Phan KL, Liberzon I, Worsley KJ, Nichols TE (2004) Nonstationary cluster-size inference with random field and permutation methods. NeuroImage 22:676–687.  https://doi.org/10.1016/j.neuroimage.2004.01.041 CrossRefPubMedGoogle Scholar
  19. Herbert MR et al (2003) Larger brain and white matter volumes in children with developmental language disorder. Dev Sci 6:F11–F22.  https://doi.org/10.1111/1467-7687.00291 CrossRefGoogle Scholar
  20. Herbert MR et al (2005) Brain asymmetries in autism and developmental language disorder: a nested whole-brain analysis. Brain 128:213–226.  https://doi.org/10.1093/brain/awh330 CrossRefPubMedGoogle Scholar
  21. Hickok G, Poeppel D (2007) The cortical organisation of speech processing. Nat Rev Neurosci 8:393–402.  https://doi.org/10.1038/nrn2113 CrossRefPubMedGoogle Scholar
  22. Jissendi P, Baudry S, Balériaux D (2008) Diffusion tensor imaging (DTI) and tractography of the cerebellar projections to prefrontal and posterior parietal cortices: a study at 3T. J Neuroradiol 35:42–50.  https://doi.org/10.1016/j.neurad.2007.11.001 CrossRefPubMedGoogle Scholar
  23. Kaufman AS, Kaufman NL (2004) Kaufman brief intelligence test, 2nd edn (KBIT-II). Pearson, BloomingtonGoogle Scholar
  24. Kenney MK, Barac-Cikoja D, Finnegan K, Jeffries N, Ludlow CL (2006) Speech perception and short-term memory deficits in persistent developmental speech disorder. Brain Lang 96:178–190CrossRefGoogle Scholar
  25. Krienen FM, Buckner RL (2009) Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex 19:2485–2497.  https://doi.org/10.1093/cercor/bhp135 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Krishnan S, Watkins KE, Bishop DV (2016) Neurobiological basis of language learning difficulties. Trends Cogn Sci 20:701–714.  https://doi.org/10.1016/j.tics.2016.06.012 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kurth F, Luders E, Pigdon L, Conti-Ramsden G, Reilly S, Morgan AT (2018) Altered gray matter volumes in language-associated regions in children with developmental language disorder and speech sound disorder. Dev Psychobiol 60(7):814–824CrossRefGoogle Scholar
  28. Law J, Rush R, Schoon I, Parsons S (2009) Modeling developmental language difficulties from school entry into adulthood: literacy, mental health, and employment outcomes. J Speech Lang Hear Res 52:1401–1416.  https://doi.org/10.1044/1092-4388(2009/08-0142) CrossRefPubMedGoogle Scholar
  29. Lee JC, Nopoulos PC, Tomblin BJ (2013) Abnormal subcortical components of the corticostriatal system in young adults with DLI: a combined structural MRI and DTI study. Neuropsychologia 51:2154–2161.  https://doi.org/10.1016/j.neuropsychologia.2013.07.011 CrossRefPubMedGoogle Scholar
  30. Leonard LB (2015) Language symptoms and their possible sources of specific language impairment. In: Bavin E, Naigles LR (eds) The Cambridge handbook of child language, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  31. Lewis BA, Freebairn LA, Taylor HG (2000) Follow-up of children with early expressive phonology disorders. J Learn Disab 33:433–444CrossRefGoogle Scholar
  32. Lewis BA, Freebairn L, Tag J, Ciesla AA, Iyengar SK, Stein CM, Taylor HG (2015) Adolescent outcomes of children with early speech sound disorders with and without language impairment. Am J Speech-Lang Pathol 24:150–163.  https://doi.org/10.1044/2014_AJSLP-14-0075 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Liégeois F, Mayes AK, Morgan AT (2014) Neural correlates of developmental speech and language disorders: evidence from neuroimaging. Curr Dev Disord Rep 1:215–227.  https://doi.org/10.1007/s40474-014-0019-1) CrossRefPubMedPubMedCentralGoogle Scholar
  34. Mariën P et al (2014) Consensus paper: language and the cerebellum: an ongoing enigma. Cerebellum 13:386–410.  https://doi.org/10.1007/s12311-013-0540-5 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Mayes AK, Reilly S, Morgan AT (2015) Neural correlates of childhood language disorder: a systematic review. Dev Med Child Neurol 57:706–717.  https://doi.org/10.1111/dmcn.12714 CrossRefPubMedGoogle Scholar
  36. McKean C et al (2017) Language outcomes at 7 years: early predictors and co-occurring difficulties. Pediatrics.  https://doi.org/10.1542/peds.2016-1684 CrossRefPubMedPubMedCentralGoogle Scholar
  37. McLeod S, Harrison LJ (2009) Epidemiology of speech and language impairment in a nationally representative sample of 4- to 5-year-old children. J Speech Lang Hear Res 52:1213–1229.  https://doi.org/10.1044/1092-4388(2009/08-0085) CrossRefPubMedGoogle Scholar
  38. Morgan AT, Bonthrone A, Liegeois F (2016) Brain basis of childhood speech and language disorders: are we closer to clinically meaningful MRI markers? Curr Opin Pediatr 28:725–730.  https://doi.org/10.1097/MOP.0000000000000420 CrossRefPubMedGoogle Scholar
  39. Morgan AT et al (2017) Who to refer for speech therapy at 4 years of age versus who to “watch and wait”? J Pediatr 185:200–204.e201.  https://doi.org/10.1016/j.jpeds.2017.02.059 CrossRefPubMedGoogle Scholar
  40. Nath AR, Beauchamp MS (2011) Dynamic changes in superior temporal sulcus connectivity during perception of noisy audiovisual speech. J Neurosci 31:1704–1714.  https://doi.org/10.1523/JNEUROSCI.4853-10.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Nicolson RI, Fawcett AJ (1990) Automaticity: a new framework for dyslexia research? Cognition 35:159–182.  https://doi.org/10.1016/0010-0277(90)90013-A CrossRefPubMedGoogle Scholar
  42. Peterson RL, McGrath LM, Smith SD, Pennington BF (2007) Neuropsychology and genetics of speech, language, and literacy disorders. Pediatr Clin North Am 54:543–561.  https://doi.org/10.1016/j.pcl.2007.02.009 CrossRefPubMedGoogle Scholar
  43. Preis S, Jäncke L, Schittler P, Huang Y, Steinmetz H (1998) Normal intrasylvian anatomical asymmetry in children with developmental language disorder. Neuropsychologia 36:849–855CrossRefGoogle Scholar
  44. Preston JL et al (2012) Functional brain activation differences in school age children with speech sound errors: speech and print processing. J Speech Lang Hear Res 55:1068–1082.  https://doi.org/10.1044/1092-4388(2011/11-0056) CrossRefPubMedPubMedCentralGoogle Scholar
  45. Preston JL et al (2014) Structural brain differences in school age children with residual speech sound errors. Brain Lang 128:25–33.  https://doi.org/10.1016/j.bandl.2013.11.001 CrossRefPubMedGoogle Scholar
  46. Pulvermüller F, Fadiga L (2010) Active perception: sensorimotor circuits as a cortical basis for language. Nat Rev Neurosci 11:351–360.  https://doi.org/10.1038/nrn2811 CrossRefGoogle Scholar
  47. Reilly S, McKean C, Morgan AT, Wake M (2015) Identifying and managing common childhood language and speech impairments. BMJ 350:h2318.  https://doi.org/10.1136/bmj.h2318 CrossRefPubMedGoogle Scholar
  48. Reilly S et al (2018) Cohort profile: the early language in victoria study (ELVS). Int J Epidemiol 47:11–12.  https://doi.org/10.1093/ije/dyx079 CrossRefPubMedGoogle Scholar
  49. Richlan F, Kronbichler M, Wimmer H (2013) Structural abnormalities in the dyslexic brain: a meta-analysis of voxel-based morphometry studies. Hum Brain Mapp.  https://doi.org/10.1002/hbm.22127 CrossRefPubMedGoogle Scholar
  50. Riva D, Giorgi C (2000) The cerebellum contributes to higher functions during development. Evidence from a series of children surgically treated for posterior fossa tumours. Brain 123:1051–1061CrossRefGoogle Scholar
  51. Rorden C, Brett M (2000) Stereotaxic display of brain regions. Behav Neurol 12:191–200CrossRefGoogle Scholar
  52. Schepers IM, Yoshor D, Beauchamp MS (2015) Electrocorticography reveals enhanced visual cortex responses to visual speech. Cereb Cortex 25:4103–4110.  https://doi.org/10.1093/cercor/bhu127 CrossRefPubMedGoogle Scholar
  53. Schoon I, Parsons S, Rush R, Law J (2010) Children’s language ability and psychosocial development: a 29-year follow-up study. Pediatrics 126:73–80.  https://doi.org/10.1542/peds.2009-3282 CrossRefGoogle Scholar
  54. Semel E, Wiig E, Secord W (2006) Clinical evaluation of language fundamentals—Australian standardised edition, 4th edn. Harcourt Assessment, SydneyGoogle Scholar
  55. Shriberg LD, Tomblin JB, McSweeny JL (1999) Prevalence of speech delay in 6-year-old children and comorbidity with language impairment. J Speech Lang Hear Res 42:1461–1481CrossRefGoogle Scholar
  56. Snowling MJ, Duff FJ, Nash HM, Hulme C (2016) Language profiles and literacy outcomes of children with resolving, emerging, or persisting language impairments. J Child Psychol Psychiatry 57:1360–1369.  https://doi.org/10.1111/jcpp.12497 CrossRefPubMedGoogle Scholar
  57. Soriano-Mas C, Pujol J, Ortiz H, Deus J, López-Sala A, Sans A (2009) Age-related brain structural alterations in children with specific language impairment. Hum Brain Mapp 30:1626–1636.  https://doi.org/10.1002/hbm.20620 CrossRefPubMedGoogle Scholar
  58. Stoodley CJ (2016) The cerebellum and neurodevelopmental disorders. Cerebellum 15:34–37.  https://doi.org/10.1007/s12311-015-0715-3 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Stoodley CJ, Schmahmann JD (2009) The cerebellum and language: evidence from patients with cerebellar degeneration. Brain Lang 110:149–153.  https://doi.org/10.1016/j.bandl.2009.07.006 CrossRefPubMedGoogle Scholar
  60. Teinonen T, Aslin RN, Alku P, Csibra G (2008) Visual speech contributes to phonetic learning in 6-month-old infants. Cognition 108:850–855.  https://doi.org/10.1016/j.cognition.2008.05.009 CrossRefPubMedGoogle Scholar
  61. Tkach JA, Chen X, Freebairn LA, Schmithorst VJ, Holland SK, Lewis BA (2011) Neural correlates of phonological processing in speech sound disorder: a functional magnetic resonance imaging study. Brain Lang 119:42–49.  https://doi.org/10.1016/j.bandl.2011.02.002 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Tomblin B (2015) Children with specific language impairment. In: Bavin EL, Naigles LR (eds) The Cambridge handbook of child language, 2nd edn. Cambridge University Press, Cambridge.  https://doi.org/10.1017/cbo9781316095829 CrossRefGoogle Scholar
  63. Ullman MT (2016) The declarative/procedural model: a neurobiological model of language. In: Hickok G, Small SL (eds) Neurobiology of language. Academic Press, Amsterdam, pp 953–968.  https://doi.org/10.1016/b978-0-12-407794-2.00076-6 CrossRefGoogle Scholar
  64. Ullman MT, Pierpont EI (2005) Specific language impairment is not specific to language: the procedural deficit hypothesis. Cortex 41:399–433.  https://doi.org/10.1016/S0010-9452(08)70276-4 CrossRefPubMedGoogle Scholar
  65. Wechsler D (1999) Wechsler abbreviated scale of intelligence. The Psychological Corporation, San AntonioGoogle Scholar
  66. Wechsler D (2011) Wechsler abbreviated scale of intelligence, 2nd edn. The Psychological Corporation, San Antonio TXGoogle Scholar
  67. Wiig E, Secord W, Semel E (2006) Clinical evaluation of language fundamentals-preschool: Australian standardised edition, 2nd edn. Harcourt Assessment, SydneyGoogle Scholar
  68. Wilkinson GS, Robertson GJ (2006) Wide range achievement test, 4th edn. Psychological Assessment Resources, LutzGoogle Scholar
  69. Woo CW, Krishnan A, Wager TD (2014) Cluster-extent based thresholding in fMRI analyses: pitfalls and recommendations. Neuroimage 91:412–419.  https://doi.org/10.1016/j.neuroimage.2013.12.058 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Worsley KJ, Andermann M, Koulis T, MacDonald D, Evans AC (1999) Detecting changes in nonisotropic images. Hum Brain Mapp 8:98–101.  https://doi.org/10.1002/(SICI)1097-0193(1999)8:2/3%3c98:AID-HBM5%3e3.0.CO;2-F CrossRefPubMedGoogle Scholar
  71. Yoon U, Fonov VS, Perusse D, Evans AC (2009) The effect of template choice on morphometric analysis of pediatric brain data. NeuroImage 45:769–777.  https://doi.org/10.1016/j.neuroimage.2008.12.046 CrossRefPubMedGoogle Scholar
  72. Zambrana IM, Pons F, Eadie P, Ystrom E (2014) Trajectories of language delay from age 3 to 5: persistence, recovery and late onset. Int J Lang Commun Disord 49:304–316.  https://doi.org/10.1111/1460-6984.12073 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Lauren Pigdon
    • 1
    • 2
  • Catherine Willmott
    • 2
    • 8
  • Sheena Reilly
    • 1
    • 7
  • Gina Conti-Ramsden
    • 1
    • 6
  • Christian Gaser
    • 9
  • Alan Connelly
    • 3
    • 4
  • Angela T. Morgan
    • 1
    • 4
    • 5
    Email author
  1. 1.Murdoch Children’s Research InstituteParkvilleAustralia
  2. 2.Turner Institute for Brain and Mental HealthMonash UniversityClaytonAustralia
  3. 3.Florey Institute of Neuroscience and Mental HealthHeidelbergAustralia
  4. 4.University of MelbourneParkvilleAustralia
  5. 5.Royal Children’s HospitalParkvilleAustralia
  6. 6.The University of ManchesterManchesterUK
  7. 7.Menzies Health Institute QueenslandGriffith UniversityMount GravattAustralia
  8. 8.Monash-Epworth Rehabilitation Research CentreMonash UniversityClaytonAustralia
  9. 9.Jena University HospitalJenaGermany

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