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White matter integrity is associated with impairments in distinct spelling mechanisms: Evidence from primary progressive aphasia

Kyriaki Neophytou1*, Andreia V. Faria2, Bronte Ficek3, Brenda Rapp1 and Kyrana Tsapkini1, 3
  • 1 Johns Hopkins University, Department of Cognitive Science, United States
  • 2 Johns Hopkins Medicine, Department of Radiology, United States
  • 3 Johns Hopkins Medicine, Department of Neurology, United States

Introduction. Previous findings suggest that spelling performance is substantially affected in Primary Progressive Aphasia (PPA) (e.g., Neophytou et al., submitted; Shim et al., 2012; Sepelyak et al., 2011). Spelling impairments in real word spelling have been associated with gray-matter lesions in ventral areas (Rapp et al., 2015; Rapcsak & Beeson, 2004). On the other hand, spelling impairments in pseudowords have been associated with grey-matter lesions in dorsal brain regions (DeMarco et al., 2017; Henry et al., 2007). However, to the best of our knowledge, no attempts have been made to determine whether these impairments in spelling performance are associated with white matter integrity. The aim of this project was to identify whether white-matter integrity as measured by functional anisotrophy (FA) values in Diffusion Tensor Imaging (DTI) are associated with spelling performance in PPA. Method. Data were collected from thirty-one participants with PPA. Responses from a spelling to dictation task with both real words and pseudowords were scored for error types. The most prominent error types that were identified for words were Phonologically Plausible Errors (PPEs), lexical substitutions, and non-PPEs. For pseudowords they were lexicalizations and non-PPEs. For DTI acquisition and analysis, we used an automated image parcellation approach: MRICloud, an atlas-based analysis developed at Johns Hopkins University. In this approach, volumetric and DTI data were parceled into approximately 200 structures, and various image parameters were quantified and analyzed for each structure We evaluated the distinction between the ventral and dorsal areas supporting spelling, using the FA values for the ventral tract, including much of the uncinate fasciculus and the extreme capsule fasciculi, and the FA values for the dorsal tract, including the supramarginal gyrus. Using linear regression models, we investigated if the FA values of the two tracts could predict each of the four error types, separately. Results. For the PPEs, the white-matter integrity of both the ventral and the dorsal areas were significant predictors: the higher the white-matter integrity in the ventral structures, the fewer the PPEs (p < .01), while the higher the white-matter integrity in the dorsal structures, the more the PPEs (p < .01). For the non-PPEs when the target was a word, only the white-matter integrity of the dorsal structures was a significant predictor: the higher the white-matter integrity in the dorsal structures, the fewer the non-PPEs (p < .05). For the other three error types, no significant effects were found. Discussion. The results suggest that when the ventral structures are intact PPA individuals make fewer PPEs, or, conversely, when the ventral structures are damaged, they make more PPEs. This suggests that, when more ventral areas are impaired, word spelling is affected and the sublexical route is utilized. On the other hand, when the dorsal structures are intact, more PPEs and fewer non-PPEs are produced, suggesting that more dorsal areas support the sublexical system. Overall, by analyzing the types of errors produced in spelling by PPA individuals we find further evidence for white-matter tracts supporting the different components of the cognitive architecture of spelling.

Acknowledgements

This work was supported by grants from the Science of Learning Institute at Johns Hopkins University and by the National Institutes of Health (NIH)/National Institute of Deafness and Communication Disorders through award R01 DC014475 to KT.

References

DeMarco, A. T., Wilson, S. M., Rising, K., Rapcsak, S. Z., & Beeson, P. M. (2017). Neural substrates of sublexical processing for spelling. Brain and language, 164, 118-128. Henry ML, et al. The role of left perisylvian cortical regions in spelling. Brain Lang. 2007;100(1):44–52. Neophytou, K., Wiley, R., Rapp, B. & Tsapkini, K. (submitted). Spelling as a single classification task in Primary Progressive Aphasia: Theoretical and Empirical Implications. Rapp, B., Purcell, J., Hillis, A. E., Capasso, R., & Miceli, G. (2015). Neural bases of orthographic long-term memory and working memory in dysgraphia. Brain, 139(2), 588-604. Rapcsak SZ, Beeson PM. The role of left posterior inferior temporal cortex in spelling. Neurology 2004; 62: 2221–9. Sepelyak, K., Crinion, J., Molitoris, J., Epstein-Peterson, Z., Bann, M., Davis, C., ... & Hillis, A. E. (2011). Patterns of breakdown in spelling in primary progressive aphasia. Cortex, 47(3), 342-352. Shim, H., Hurley, R. S., Rogalski, E., & Mesulam, M. M. (2012). Anatomic, clinical, and neuropsychological correlates of spelling errors in primary progressive aphasia. Neuropsychologia, 50(8), 1929-1935.

Keywords: primary progressive aphasia, DTI (diffusion tensor imaging), spelling, ventral-dorsal pathways, Fractional Anisotropy (FA)

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: Neophytou K, Faria AV, Ficek B, Rapp B and Tsapkini K (2019). White matter integrity is associated with impairments in distinct spelling mechanisms: Evidence from primary progressive aphasia. Front. Hum. Neurosci. Conference Abstract: Academy of Aphasia 57th Annual Meeting. doi: 10.3389/conf.fnhum.2019.01.00119

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Received: 07 May 2019; Published Online: 09 Oct 2019.

* Correspondence: Ms. Kyriaki Neophytou, Johns Hopkins University, Department of Cognitive Science, Baltimore, United States, kneophy1@jhu.edu