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Structural disconnection maps associated with language impairment in chronic aphasia

Anne Billot1*, Michel Thiebaut De Schotten2, 3, 4, Todd Parrish5, 6, Cynthia K. Thompson5, 7*, Brenda Rapp8, David Caplan9 and Swathi Kiran10
  • 1 Division of Graduate Medical Sciences, Boston University, United States
  • 2 Sorbonne Universités, France
  • 3 INSERM U1127 Institut du Cerveau et de la Moelle épinière (ICM), France
  • 4 Université de Bordeaux, France
  • 5 Feinberg School of Medicine, Northwestern University, United States
  • 6 Department of Radiology, Feinberg School of Medicine, Northwestern University, United States
  • 7 Center for the Neurobiology of Language Recovery, Northwestern University, United States
  • 8 Department of Cognitive Science, Krieger School of Arts and Sciences, Johns Hopkins University, United States
  • 9 Massachusetts General Hospital, Harvard Medical School, United States
  • 10 Department of Speech, Language and Hearing Sciences, Boston University, United States

The analysis of residual white matter connections between brain regions is essential to understand language impairment in post-stroke aphasia [1]. Tractography studies have found that white matter integrity is a good predictor of language outcomes after stroke [2]. However, few studies have investigated the relationship between seemingly spared but directly disconnected white matter pathways and language impairments in chronic aphasia. Probabilistic maps of disconnection based on anatomical connectomes of healthy controls are a complementary method to measure the impact of the lesion on neuronal circuits [3]. This project examined the relationship between language deficits and the degree of structural disconnections in the brain of people with chronic aphasia. This study includes 76 individuals with chronic aphasia resulting from a single left-hemisphere stroke. Participants were recruited from three sites (Boston, Johns Hopkins, and Northwestern Universities) and underwent an MRI and DTI imaging and an extensive language assessment (Western Aphasia Battery-Revised - WAB [4]; Northwestern Assessment of Verbs and Sentences - NAVS, [5]; Psycholinguistic Assessments of Language Processing - PALPA [6]). 75 individuals have completed NAVS (sentence production) and 74 have completed PALPA. Probability maps of white matter tracts' disconnection were computed for each participant with the “disconnectome map” tool of the BCBToolkit [3] using 178 healthy controls diffusion weighting imaging datasets (7T, www.humanconnectomeproject.org). For each individual with aphasia, the lesion mask was registered in MNI space and used as a seed to produce the tractography of healthy controls’ fibers passing through the lesion. Then, at each voxel, tractographies from healthy controls were binarized and summed to produce a percentage overlap map, and consequently, the probability of disconnection (range 0-100%). A threshold of 50% (50% of controls had tracts passing through the lesion) was applied for this study. Nonparametric permutation analyses and threshold-free cluster enhancement technique were used to evaluate the correlation between the probability of white matter disconnection and each language score (WAB: aphasia severity, auditory verbal comprehension, repetition, naming; NAVS: sentence comprehension, sentence production priming test; PALPA-40: spelling). Demographic variables and lesion size were included as covariates of no interest in the general linear model implemented in Randomise (FSL package, [7]). Family-wise error rate was controlled at p<0.001 (Figure 1). Atlasquery tool (FSL package, [7]) was used to identify disconnected tracts significantly correlated with each language score. Tracts with a probability of overlapping with more than 1% of the statistical mapping of the disconnections were selected. Table 1 shows that disconnected tracts contributing most to all language impairments included in this study were the left external capsule, the left posterior limb of the internal capsule, the left cerebral peduncle and the middle cerebellar peduncle (p=0.001). In addition, specific linguistic domain scores were correlated with different disconnected tracts including the Left IFOF, ILF and SLF (Table 1). This study identified white matter tracts’ disconnections associated with aphasia severity and the degree of impairment in verbal comprehension, repetition, naming, sentence processing, and spelling. Disconnectome mapping confirms previous findings showing that structural damage is related to language outcomes beyond cortical necrosis.

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Acknowledgements

This work was supported by the NIH/NIDCD Clinical Research Center Grant, P50DC012283, and the Center for the Neurobiology of Language Recovery.

References

[1] Catani, M., & Mesulam, M. (2008). The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. cortex, 44(8), 953-961. [2] Kiran, S., & Thompson, C. K. (2019). Neuroplasticity of Language Networks in Aphasia: Advances, Updates and Future Challenges. Frontiers in neurology, 10, 295. [3] Foulon, C., Cerliani, L., Kinkingnehun, S., Levy, R., Rosso, C., Urbanski, M., ... & Thiebaut de Schotten, M. (2018). Advanced lesion symptom mapping analyses and implementation as BCBtoolkit. GigaScience, 7(3), giy004. [4] Kertesz, A. (2007). WAB-R: Western aphasia battery-revised. PsychCorp. [5] Thompson, C. K. (2012). Northwestern Assessment of Verbs and Sentences (NAVS). [6] Kay, J., Lesser, R., & Coltheart, M. (1996). Psycholinguistic assessments of language processing in aphasia (PALPA): An introduction. Aphasiology, 10(2), 159-180. [7] Winkler, A. M., Ridgway, G. R., Webster, M. A., Smith, S. M., & Nichols, T. E. (2014). Permutation inference for the general linear model. Neuroimage, 92, 381-397.

Keywords: Aphasia, Stroke, White matter (WM), Language, Disconnection, Magnetic Resonance Image (MRI)

Conference: Academy of Aphasia 57th Annual Meeting, Macau, Macao, SAR China, 27 Oct - 29 Oct, 2019.

Presentation Type: Platform presentation

Topic: Eligible for student award

Citation: Billot A, Thiebaut De Schotten M, Parrish T, Thompson CK, Rapp B, Caplan D and Kiran S (2019). Structural disconnection maps associated with language impairment in chronic aphasia. Front. Hum. Neurosci. Conference Abstract: Academy of Aphasia 57th Annual Meeting. doi: 10.3389/conf.fnhum.2019.01.00040

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Received: 06 May 2019; Published Online: 09 Oct 2019.

* Correspondence:
Mx. Anne Billot, Division of Graduate Medical Sciences, Boston University, Boston, Massachusetts, 02118, United States, abillot@bu.edu
Prof. Cynthia K Thompson, Center for the Neurobiology of Language Recovery, Northwestern University, Evanston, Illinois, 60208, United States, ckthom@northwestern.edu