Brain Topography

, Volume 31, Issue 2, pp 300–310 | Cite as

Altered Structure and Intrinsic Functional Connectivity in Post-stroke Aphasia

Original Paper
  • 109 Downloads

Abstract

Previous studies have demonstrated that alterations of gray matter exist in post-stroke aphasia (PSA) patients. However, so far, few studies combined structural alterations of gray matter volume (GMV) and intrinsic functional connectivity (iFC) imbalances of resting-state functional MRI to investigate the mechanism underlying PSA. The present study investigated specific regions with GMV abnormality in patients with PSA (n = 17) and age- and sex- matched healthy controls (HCs, n = 20) using voxel-based morphometry. In addition, we examined whether there is a link between abnormal gray matter and altered iFC. Furthermore, we explored the correlations between abnormal iFC and clinical scores in aphasic patients. We found significantly increased GMV in the right superior temporal gyrus, right inferior parietal lobule (IPL)/supramarginal gyrus (SMG), and left middle occipital gyrus. Decreased GMV was found in the right caudate gyrus, bilateral thalami in PSA patients. Patients showed increased remote interregional FC between the right IPL/SMG and right precuneus, right angular gyrus, right superior occipital gyrus; while reduced FC in the right caudate gyrus and supplementary motor area, dorsolateral superior frontal gyrus. Moreover, iFC strength between the left middle occipital gyrus and the left orbital middle frontal gyrus was positively correlated with the performance quotient. We suggest that GMV abnormality contributes to interregional FC in PSA. These results may provide useful information to understand the pathogenesis of post-stroke aphasia.

Keywords

Gray matter volume Intrinsic functional connectivity Post-stroke aphasia Resting-state 

Abbreviations

ABC

Aphasia battery of Chinese

AQ

Aphasia quotient

CQ

Cortical quotient

FD

Frame-wise displacement

fMRI

Functional magnetic resonance imaging

GMV

Gray matter volume

iFC

Intrinsic functional connectivity

PQ

Performance quotient

PSA

Post-stroke aphasia

VBM

Voxel-based morphometry

Notes

Acknowledgements

We thank the radiologist Ying Liu (Y.L.) from the Hospital of Fuzhou for manually tracing the outline of the lesion. This work was supported by the 863 project (2015AA020505), Natural Science Foundation of China (61533006 and 81471653), China Postdoctoral Science Foundation (2013M532229), Fundamental Research Funds for the Central Universities (ZYGX2013Z004), Sichuan provincial health and family planning commission research project (16PJ051), and the project of the Science and Technology Department in Sichuan province (2017JY0094).

Author Contributions

DY, WL, and HC designed the study. MY, PY, YF and JL contributed to data collection. MY, PY, YF and JL contributed to data analysis, data interpretation, and manuscript preparation. All authors read and approved the final manuscript.

References

  1. Abdullaev YG, Bechtereva NP, Melnichuk KV (1998) Neuronal activity of human caudate nucleus and prefrontal cortex in cognitive tasks. Behav Brain Res 97:159–177CrossRefPubMedGoogle Scholar
  2. Agosta F, Galantucci S, Valsasina P, Canu E, Meani A, Marcone A et al (2014) Disrupted brain connectome in semantic variant of primary progressive aphasia. Neurobiol Aging 35:2646–2655CrossRefPubMedGoogle Scholar
  3. Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. Neuroimage 11:805–821CrossRefPubMedGoogle Scholar
  4. Ashizuka A, Mima T, Sawamoto N, Aso T, Oishi N, Sugihara G et al (2015) Functional relevance of the precuneus in verbal politeness. Neurosci Res 91:48–56CrossRefPubMedGoogle Scholar
  5. Berthier ML (2005) Poststroke aphasia: epidemiology, pathophysiology and treatment. Drugs Aging 22:163–182CrossRefPubMedGoogle Scholar
  6. Binder JR, Desai RH, Graves WW, Conant LL (2009) Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex 19:2767–2796CrossRefPubMedPubMedCentralGoogle Scholar
  7. Braun AR, Guillemin A, Hosey L, Varga M (2001) The neural organization of discourse—an (H2O)-O-15-PET study of narrative production in English and American sign language. Brain 124:2028–2044CrossRefPubMedGoogle Scholar
  8. Brett M, Leff AP, Rorden C, Ashburner J (2001) Spatial normalization of brain images with focal lesions using cost function masking. Neuroimage 14:486–500CrossRefPubMedGoogle Scholar
  9. Broyd SJ, Demanuele C, Debener S, Helps SK, James CJ, Sonuga-Barke EJS (2009) Default-mode brain dysfunction in mental disorders: a systematic review. Neurosci Biobehav Rev 33:279–296CrossRefPubMedGoogle Scholar
  10. Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583CrossRefPubMedGoogle Scholar
  11. Chao-Gan Y, Yu-Feng Z (2010) DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fmRI. Front Syst Neurosci 4:13–13PubMedPubMedCentralGoogle Scholar
  12. Charney JZ (1981) Aphasia and associated disorders: taxonomy, localization, and recovery. JAMA 245:78CrossRefGoogle Scholar
  13. Chou T-L, Booth JR, Bitan T, Burman DD, Bigio JD, Cone NE et al (2006a) Developmental and skill effects on the neural correlates of semantic processing to visually presented words. Hum Brain Mapp 27:915–924CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chou TL, Booth JR, Burman DD, Bitan T, Bigio JD, Lu D et al (2006b) Developmental changes in the neural correlates of semantic processing. Neuroimage 29:1141–1149CrossRefPubMedGoogle Scholar
  15. Crosson B, Benefield H, Cato MA, Sadek JR, Moore AB, Wierenga CE et al (2003) Left and right basal ganglia and frontal activity during language generation: contributions to lexical, semantic, and phonological processes. J Int Neuropsychol Soc 9:1061–1077PubMedGoogle Scholar
  16. Cuadra MB, Cammoun L, Butz T, Cuisenaire O, Thiran JP (2005) Comparison and validation of tissue modelization and statistical classification methods in T1-weighted MR brain images. IEEE Trans Med Imaging 24:1548–1565CrossRefPubMedGoogle Scholar
  17. Dong JW, Brennan NMP, Izzo G, Peck KK, Holodny AI (2016) fMRI activation in the middle frontal gyrus as an indicator of hemispheric dominance for language in brain tumor patients: a comparison with Broca’s area. Neuroradiology 58:513–520CrossRefPubMedPubMedCentralGoogle Scholar
  18. Dronkers NF (1996) A new brain region for coordinating speech articulation. Nature 384:159–161CrossRefPubMedGoogle Scholar
  19. Dronkers NF, Wilkins DP, Van Valin RD Jr, Redfern BB, Jaeger JJ (2004) Lesion analysis of the brain areas involved in language comprehension. Cognition 92:145–177CrossRefPubMedGoogle Scholar
  20. Ellis C, Simpson AN, Bonilha H, Mauldin PD, Simpson KN (2012) The one-year attributable cost of poststroke aphasia. Stroke 43:1429–1431CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102:9673–9678CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fridriksson J, Richardson JD, Fillmore P, Cai B (2012) Left hemisphere plasticity and aphasia recovery. Neuroimage 60:854–863CrossRefPubMedGoogle Scholar
  23. Gao SR, Chu YF, Shi S, Peng Q, Dai SD, Wang YMH (1992) A standardization research of the aphasia battery of Chinese. Chin Mental Health J 6:125–128Google Scholar
  24. Geva S, Baron JC, Jones PS, Price CJ, Warburton EA (2012) A comparison of VLSM and VBM in a cohort of patients with post-stroke aphasia. Neuroimage Clin 1:37–47CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ghosh S, Basu A, Kumaran SS, Khushu S (2010) Functional mapping of language networks in the normal brain using a word-association task. Indian J Radiol Imaging 20:182–187CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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 56:90–100CrossRefPubMedGoogle Scholar
  27. Good CD, Johnsrude IS, Ashburner J, Henson RNA, Friston KJ, Frackowiak RSJ (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14:21–36CrossRefPubMedGoogle Scholar
  28. Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19:72–78CrossRefPubMedGoogle Scholar
  29. Hagmann P, Sporns O, Madan N, Cammoun L, Pienaar R, Wedeen VJ et al (2010) White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci USA 107:19067–19072CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hartwigsen G, Baumgaertner A, Price CJ, Koehnke M, Ulmer S, Siebner HR (2010) Phonological decisions require both the left and right supramarginal gyri. Proc Natl Acad Sci USA 107:16494–16499CrossRefPubMedPubMedCentralGoogle Scholar
  31. Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R et al (2009) Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci USA 106:2035–2040CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ji GJ, Zhang Z, Xu Q, Zang YF, Liao W, Lu G (2014) Generalized tonic-clonic seizures: aberrant interhemispheric functional and anatomical connectivity. Radiology 271:839–847CrossRefPubMedGoogle Scholar
  33. Johnson MD, Ojemann GA (2000) The role of the human thalamus in language and memory: evidence from electrophysiological studies. Brain Cogn 42:218–230CrossRefPubMedGoogle Scholar
  34. Jonas S (1982) The thalamus and aphasia, including transcortical aphasia: a review. J Commun Disord 15:31–41CrossRefPubMedGoogle Scholar
  35. Just MA, Cherkassky VL, Keller TA, Minshew NJ (2004) Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain 127:1811–1821CrossRefPubMedGoogle Scholar
  36. Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA (2006) Sentence comprehension in autism: thinking in pictures with decreased functional connectivity. Brain 129:2484–2493CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kochunov P, Thompson PM, Lancaster JL, Bartzokis G, Smith S, Coyle T et al (2007) Relationship between white matter fractional anisotropy and other indices of cerebral health in normal aging: tract-based spatial statistics study of aging. Neuroimage 35:478–487CrossRefPubMedGoogle Scholar
  38. Liao W, Xu Q, Mantini D, Ding J, Machado-de-Sousa JP, Hallak JE et al (2011a) Altered gray matter morphometry and resting-state functional and structural connectivity in social anxiety disorder. Brain Res 1388:167–177CrossRefPubMedGoogle Scholar
  39. Liao W, Zhang Z, Pan Z, Mantini D, Ding J, Duan X et al (2011b) Default mode network abnormalities in mesial temporal lobe epilepsy: a study combining fMRI and DTI. Hum Brain Mapp 32:883–895CrossRefPubMedGoogle Scholar
  40. Liao W, Yu Y, Miao HH, Feng YX, Ji GJ, Feng JH (2017) Inter-hemispheric intrinsic connectivity as a neuromarker for the diagnosis of boys with Tourette syndrome. Mol Neurobiol 54:2781–2789CrossRefPubMedGoogle Scholar
  41. Liu L, Luo X-G, Dy C-L, Ren Y, Feng Y, Yu H-M et al (2015) Characteristics of language impairment in Parkinson’s disease and its influencing factors. Transl Neurodegener 4:2–2CrossRefPubMedPubMedCentralGoogle Scholar
  42. Long Z, Xu Q, Miao HH, Yu Y, Ding MP, Chen H et al (2017) Thalamocortical dysconnectivity in paroxysmal kinesigenic dyskinesia: Combining functional magnetic resonance imaging and diffusion tensor imaging. Mov Disord 32:592–600CrossRefPubMedGoogle Scholar
  43. Lu J, Wu J, Yao C, Zhuang D, Qiu T, Hu X et al (2013) Awake language mapping and 3-Tesla intraoperative MRI-guided volumetric resection for gliomas in language areas. J Clin Neurosci 20:1280–1287CrossRefPubMedGoogle Scholar
  44. Martensson F, Roll M, Lindgren M, Apt P, Horne M (2014) Sensory-specific anomic aphasia following left occipital lesions: data from free oral descriptions of concrete word meanings. Neurocase 20:192–207CrossRefPubMedGoogle Scholar
  45. Menke R, Meinzer M, Kugel H, Deppe M, Baumgaertner A, Schiffbauer H et al (2009) Imaging short- and long-term training success in chronic aphasia. BMC Neurosci 10:118CrossRefPubMedPubMedCentralGoogle Scholar
  46. Musso M, Weiller C, Kiebel S, Muller SP, Bulau P, Rijntjes M (1999) Training-induced brain plasticity in aphasia. Brain 122:1781–1790CrossRefPubMedGoogle Scholar
  47. Nair VA, Young BM, La C, Reiter P, Nadkarni TN, Song J et al (2015) Functional connectivity changes in the language network during stroke recovery. Ann Clin Transl Neurol 2:185–195CrossRefPubMedPubMedCentralGoogle Scholar
  48. Ogar JM, Baldo JV, Wilson SM, Brambati SM, Miller BL, Dronkers NF et al (2011) Semantic dementia and persisting Wernicke’s aphasia: Linguistic and anatomical profiles. Brain Lang 117:28–33CrossRefPubMedPubMedCentralGoogle Scholar
  49. Oliver RT, Geiger EJ, Lewandowski BC, Thompson-Schill SL (2009) Remembrance of things touched: How sensorimotor experience affects the neural instantiation of object form. Neuropsychologia 47:239–247CrossRefPubMedGoogle Scholar
  50. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154CrossRefPubMedGoogle Scholar
  51. Price CJ (2010) The anatomy of language: a review of 100 fMRI studies published in 2009. Ann NY Acad Sci 1191:62–88CrossRefPubMedGoogle Scholar
  52. Price CJ, Devlin JT (2003) The myth of the visual word form area. Neuroimage 19:473–481CrossRefPubMedGoogle Scholar
  53. Radulescu E, Minati L, Ganeshan B, Harrison NA, Gray MA, Beacher FDCC et al (2013) Abnormalities in fronto-striatal connectivity within language networks relate to differences in grey-matter heterogeneity in Asperger syndrome. Neuroimage Clin 2:716–726CrossRefPubMedPubMedCentralGoogle Scholar
  54. Raposo A, Moss HE, Stamatakis EA, Tyler LK (2006) Repetition suppression and semantic enhancement: An investigation of the neural correlates of priming. Neuropsychologia 44:2284–2295CrossRefPubMedGoogle Scholar
  55. Sakai KL, Nauchi A, Tatsuno Y, Hirano K, Muraishi Y, Kimura M et al (2009) Distinct roles of left inferior frontal regions that explain individual differences in second language acquisition. Hum Brain Mapp 30:2440–2452CrossRefPubMedGoogle Scholar
  56. Sims JA, Kapse K, Glynn P, Sandberg C, Tripodis Y, Kiran S (2016) The relationships between the amount of spared tissue, percent signal change, and accuracy in semantic processing in aphasia. Neuropsychologia 84:113–126CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sollmann N, Tanigawa N, Ringel F, Zimmer C, Meyer B, Krieg SM (2014) Language and its right-hemispheric distribution in healthy brains: an investigation by repetitive transcranial magnetic stimulation. Neuroimage 102:776–788CrossRefPubMedGoogle Scholar
  58. Stebbins GT, Nyenhuis DL, Wang C, Cox JL, Freels S, Bangen K et al (2008) Gray matter atrophy in patients with ischemic stroke with cognitive impairment. Stroke 39:785–793CrossRefPubMedGoogle Scholar
  59. Turken AU, Dronkers NF (2011) The neural architecture of the language comprehension network: converging evidence from lesion and connectivity analyses. Front Syst Neurosci 5:1–1CrossRefPubMedPubMedCentralGoogle Scholar
  60. van Hees S, McMahon K, Angwin A, de Zubicaray G, Read S, Copland DA (2014a) Changes in white matter connectivity following therapy for anomia post stroke. Neurorehabil Neural Repair 28:325–334CrossRefPubMedGoogle Scholar
  61. van Hees S, McMahon K, Angwin A, de Zubicaray G, Read S, Copland DA (2014b) A functional MRI study of the relationship between naming treatment outcomes and resting state functional connectivity in post-stroke aphasia. Hum Brain Mapp 35:3919–3931CrossRefPubMedGoogle Scholar
  62. Wang X, Wang M, Wang W, Liu H, Tao J, Yang C et al (2014) Resting state brain default network in patients with motor aphasia resulting from cerebral infarction. Chin Sci Bull 59:4069–4076CrossRefGoogle Scholar
  63. Wise RJS, Greene J, Buchel C, Scott SK (1999) Brain regions involved in articulation. The Lancet 353:1057–1061CrossRefGoogle Scholar
  64. Xu Y, Lin Q, Han Z, He Y, Bi Y (2016) Intrinsic functional network architecture of human semantic processing: modules and hubs. Neuroimage 132:542–555CrossRefPubMedGoogle Scholar
  65. Yang M, Li J, Li Y, Li R, Pang Y, Yao D et al (2016a) Altered intrinsic regional activity and interregional functional connectivity in post-stroke aphasia. Sci Rep 6:24803CrossRefPubMedPubMedCentralGoogle Scholar
  66. Yang M, Li J, Yao D, Chen H (2016b) Disrupted intrinsic local synchronization in poststroke aphasia. Medicine 95:e3101CrossRefPubMedPubMedCentralGoogle Scholar
  67. Yang M, Li Y, Li J, Yao D, Liao W, Chen H (2017) Beyond the arcuate fasciculus: damage to ventral and dorsal language pathways in aphasia. Brain Topogr 30:249–256CrossRefPubMedGoogle Scholar
  68. Zeng LL, Wang D, Fox MD, Sabuncu M, Hu D, Ge M et al (2014) Neurobiological basis of head motion in brain imaging. Proc Natl Acad Sci USA 111:6058–6062CrossRefPubMedPubMedCentralGoogle Scholar
  69. Zhang Z, Liao W, Chen H, Mantini D, Ding JR, Xu Q et al (2011) Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy. Brain 134:2912–2928CrossRefPubMedGoogle Scholar
  70. Zhu D, Chang J, Freeman S, Tan Z, Xiao J, Gao Y et al (2014) Changes of functional connectivity in the left frontoparietal network following aphasic stroke. Front Behav Neurosci 8:167CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Key Laboratory for NeuroInformation of Ministry of Education, Center for Information in BioMedicine, School of Life Science and TechnologyUniversity of Electronic Science and Technology of ChinaChengduPeople’s Republic of China
  2. 2.Department of Stomatologythe Fourth People’s Hospital of ChengduChengduPeople’s Republic of China

Personalised recommendations