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White matter pathway supporting phonological encoding in speech production: a multi-modal imaging study of brain damage patients

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Abstract

In speech production, an important step before motor programming is the retrieval and encoding of the phonological elements of target words. It has been proposed that phonological encoding is supported by multiple regions in the left frontal, temporal and parietal regions and their underlying white matter, especially the left arcuate fasciculus (AF) or superior longitudinal fasciculus (SLF). It is unclear, however, whether the effects of AF/SLF are indeed related to phonological encoding for output and whether there are other white matter tracts that also contribute to this process. We comprehensively investigated the anatomical connectivity supporting phonological encoding in production by studying the relationship between the integrity of all major white matter tracts across the entire brain and phonological encoding deficits in a group of 69 patients with brain damage. The integrity of each white matter tract was measured both by the percentage of damaged voxels (structural imaging) and the mean fractional anisotropy value (diffusion tensor imaging). The phonological encoding deficits were assessed by various measures in two oral production tasks that involve phonological encoding: the percentage of nonword (phonological) errors in oral picture naming and the accuracy of word reading aloud with word comprehension ability regressed out. We found that the integrity of the left SLF in both the structural and diffusion tensor imaging measures consistently predicted the severity of phonological encoding impairment in the two phonological production tasks. Such effects of the left SLF on phonological production remained significant when a range of potential confounding factors were considered through partial correlation, including total lesion volume, demographic factors, lesions on phonological-relevant grey matter regions, or effects originating from the phonological perception or semantic processes. Our results therefore conclusively demonstrate the central role of the left SLF in phonological encoding in speech production.

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Notes

  1. Note that although AF and SLF have been traditionally viewed as synonyms depicting the same tract (see Dick and Tremblay 2012 for a review), there are recent debates about their distinctions (Makris et al. 2005; Petrides and Pandya 2009; Schmahmann et al. 2007). We for now do not distinguish them to cover studies about these tracts more comprehensively and defer their potential differences to the discussion.

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Acknowledgments

We thank Litao Zhu for help with imaging methodology, Xiaodong Liu for help with statistical analysis and all BNU-CNLab members for data collection and imaging preprocessing, in particular Yangwen Xu, Fangson Liu and Jing Chen. We are also grateful to all research participants. This study was funded by 973 Program (2013CB837300; 2014CB846100), Major Project of National Social Science Foundation (11&ZD186), NSFC (31171073; 31222024; 31221003; 81071149; 81271548; 81371535; 31271115; 81322021), Beijing Natural Science Foundation (Z111107067311036), NCET (12-0055; 12-0065), Beijing Nova Program (Z121110002512032), Beijing New Medical Discipline Based Group (100270569). Author contributions: ZH, YB and LS designed research; ZH and YM performed research; ZH, YM and GG analyzed data; RH designed imaging sequence; LS recruited and screened patients; ZH and YB wrote the paper.

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Authors and Affiliations

  1. State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China

    Zaizhu Han, Yujun Ma, Gaolang Gong & Yanchao Bi

  2. Department of Psychology, Henan University, Kaifeng, 475000, China

    Yujun Ma

  3. Center for the Study of Applied Psychology, Key Laboratory of Mental Health and Cognitive Science of Guangdong Province, School of Psychology, South China Normal University, Guangzhou, 510631, China

    Ruiwang Huang

  4. Department of Neuro-rehabilitation, Rehabilitation College of Capital Medical University and China Rehabilitation Research Center, Beijing, 100068, China

    Luping Song

  5. Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing, 100875, China

    Zaizhu Han, Gaolang Gong & Yanchao Bi

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  1. Zaizhu Han
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  2. Yujun Ma
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  3. Gaolang Gong
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  4. Ruiwang Huang
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  5. Luping Song
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  6. Yanchao Bi
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Correspondence to Zaizhu Han or Luping Song.

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Z. Han, Y. Ma are co-first authors.

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Han, Z., Ma, Y., Gong, G. et al. White matter pathway supporting phonological encoding in speech production: a multi-modal imaging study of brain damage patients. Brain Struct Funct 221, 577–589 (2016). https://doi.org/10.1007/s00429-014-0926-2

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  • DOI: https://doi.org/10.1007/s00429-014-0926-2

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