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Convergence of Heteromodal Lexical Retrieval in the Lateral Prefrontal Cortex

Alexander A. Aabedi, Sofia Kakaizada, Jacob S. Young, Olivia Wiese, Claudia Valdivia, Mitchel S. Berger, Daniel H. Weissman, David Brang, Shawn L. Hervey-Jumper
doi: https://doi.org/10.1101/2020.11.30.405746
Alexander A. Aabedi
1Department of Neurological Surgery, University of California San Francisco, California, 94143
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Sofia Kakaizada
1Department of Neurological Surgery, University of California San Francisco, California, 94143
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Jacob S. Young
1Department of Neurological Surgery, University of California San Francisco, California, 94143
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Olivia Wiese
2Department of Psychology, University of Michigan at Ann Arbor, Michigan, 48109
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Claudia Valdivia
1Department of Neurological Surgery, University of California San Francisco, California, 94143
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Mitchel S. Berger
1Department of Neurological Surgery, University of California San Francisco, California, 94143
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Daniel H. Weissman
2Department of Psychology, University of Michigan at Ann Arbor, Michigan, 48109
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David Brang
2Department of Psychology, University of Michigan at Ann Arbor, Michigan, 48109
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Shawn L. Hervey-Jumper
1Department of Neurological Surgery, University of California San Francisco, California, 94143
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  • For correspondence: shawn.hervery-jumper@ucsf.edu
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Abstract

Lexical retrieval requires selecting and retrieving the most appropriate word from the lexicon to express a desired concept. Prior studies investigating the neuroanatomic underpinnings of lexical retrieval used lesion models that rely on stereotyped vascular distributions, functional neuroimaging methods that lack causal certainty, or awake brain mapping that is typically limited to narrow cortical exposures. Further, few studies have probed lexical retrieval with tasks other than picture naming and when non-picture naming lexical retrieval tasks have been applied, both convergent and divergent models emerged. Because of this existing controversy, we set out to test the hypothesis that cortical and subcortical brain regions specifically involved in lexical retrieval in response to visual and auditory stimuli represent overlapping neural systems. Fifty-three patients with dysnomic aphasia due to dominant-hemisphere brain tumors performed four language tasks: picture naming, auditory naming, text reading, and describing line drawings with correct syntax. A subset of participants also underwent the Quick Aphasia Battery which provides a validated measure of lexical retrieval via the word finding subtest. Generalized linear modeling and principal components analysis revealed multicollinearity between picture naming, auditory naming, and word finding, implying redundancies between the linguistic measures. Support vector regression lesion-symptom mapping across participants was used to model accuracies on each of the four language tasks. Picture naming and auditory naming survived cluster-level corrections. Specifically, lesions within overlapping clusters of 8,333 voxels and 21,512 voxels in the left lateral PFC were predictive of impaired picture naming and auditory naming, respectively. These data indicate a convergence of heteromodal lexical retrieval within the PFC.

Importance of the Study Lexical retrieval (i.e., selecting and retrieving words to convey desired concepts) is a crucial component of language processing. However, existing studies of the neuroanatomic underpinnings of lexical retrieval lack causal relationships and have provided conflicting evidence, suggesting both convergent and divergent models. In order to resolve these conflicting models, we used lesion-symptom mapping to investigate lexical retrieval in 53 patients with dominant-hemisphere brain tumors. We observed significant associations between performance on visual and auditory naming tasks. Further, performance on these tasks predicted performance on a validated neuropsychological measure of lexical retrieval. Critically, multivariate, nonparametric lesion-symptom mapping within a brain tumor framework revealed that lesions in overlapping regions of the left lateral prefrontal cortex (PFC) predict impaired visual and auditory naming. In a clinical context, this approach to identifying causal brain-behavior relationships could help to guide brain tumor therapies such as cytoreductive surgery and supportive rehabilitation services.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Financial Disclosures: The authors declare no competing financial interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted December 01, 2020.
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Convergence of Heteromodal Lexical Retrieval in the Lateral Prefrontal Cortex
Alexander A. Aabedi, Sofia Kakaizada, Jacob S. Young, Olivia Wiese, Claudia Valdivia, Mitchel S. Berger, Daniel H. Weissman, David Brang, Shawn L. Hervey-Jumper
bioRxiv 2020.11.30.405746; doi: https://doi.org/10.1101/2020.11.30.405746
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Convergence of Heteromodal Lexical Retrieval in the Lateral Prefrontal Cortex
Alexander A. Aabedi, Sofia Kakaizada, Jacob S. Young, Olivia Wiese, Claudia Valdivia, Mitchel S. Berger, Daniel H. Weissman, David Brang, Shawn L. Hervey-Jumper
bioRxiv 2020.11.30.405746; doi: https://doi.org/10.1101/2020.11.30.405746

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