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Dissociating Grammatical Categories in Temporal and Perisylvian networks: Evidence from Neurodegenerative Disease

Sladjana Lukic1*, Valentina Borghesani1, Wendy Shwe1, Elizabeth Weis1, Zachary A. Miller1, Jessica Deleon1, John Neuhaus1, Bruce L. Miller1 and Maria L. Gorno-Tempini1
  • 1 Memory and Aging Center, University of California at San Francisco, United States

Introduction. A frequent symptom across neurodegenerative disorders is difficulty with naming, which differentially can affect grammatical categories such as nouns (i.e., naming objects) or verbs (i.e., naming actions) (Cotteli et al., 2006; Hardy et al., 2016, Hillis et al., 2006, Thompson et al., 2012). Successful naming relies on multiple cognitive processes supported by brain networks which can be selectively disrupted in different disorders. It is currently debated whether different patterns of impairment in naming nouns and verbs can be related to distinct patterns of atrophy in neurodegenerative diseases. This study aims to investigate the neural correlates of naming impairments in a large group of patients with frontotemporal dementia-spectrum disorders (FTD) and Alzheimer’s disease (AD). Methods. One hundred sixty-four subjects (30 nonfluent/agrammatic, 30 semantic and 18 logopenic variants of primary progressive aphasia (PPA); 40 behavioral variant FTD; 16 AD; 30 healthy controls) underwent an extensive neuropsychological battery, an experimental noun and verb naming test (Thompson et al., 2012), and structural MRI scanning. We compared overall and category-specific naming performances across clinical groups to investigate syndrome-specific patterns of naming deficits. We then correlated naming scores with cortical thickness across all subjects using whole-brain surface-based morphometry in SPM. Age, gender, and disease severity were included as covariates in all analyses. Significance was set at p < 0.05 corrected for multiple comparisons. Results. All clinical groups had significantly lower overall naming performance relative to healthy controls. Semantic PPA patients were more impaired than other FTD and AD groups. Semantic PPA showed a grammatical category effect by naming significantly fewer nouns than verbs, whereas nonfluent/agrammatic PPA showed the opposite dissociation by naming fewer verbs than nouns. Neuroimaging results showed that overall naming significantly correlated with cortical thickness in the left temporo-parietal areas. Performance on nouns correlated with left anterior temporal regions, while performance on verbs correlated with the left inferior frontal, inferior parietal (supramarginal gyrus) and posterior temporal regions (Figure 1). We then performed a post-hoc analysis on behavioral data to investigate the cognitive processes underlying noun and verb naming deficits. Based on the neuroimaging results, we hypothesized that noun and verb naming scores would correlate with measures of semantic and lexico-syntactic processes respectively. We found that scores on nouns and verbs significantly correlated with lower semantic abilities, while verb naming only correlated with lower syntactic abilities. Conclusions. Taken together, these findings suggest that different neuro-cognitive mechanisms support naming of specific grammatical categories in neurodegenerative diseases. Specifically, nouns appear to rely on semantic processes occurring in the left anterior temporal lobe, while verbs on syntactic and lexical processes in the left perisylvian regions. These improve our fundamental understanding of the neural basis for spared and impaired naming processes.

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References

[1] Cotelli, M., Borroni, B., Manenti, R., Alberici, A., Calabria, M., Agosti, C., ... & Zanetti, O. (2006). Action and object naming in frontotemporal dementia, progressive supranuclear palsy, and corticobasal degeneration. Neuropsychology, 20(5), 558. [2] Hardy, C. J., Buckley, A. H., Downey, L. E., Lehmann, M., Zimmerer, V. C., Varley, R. A., ... & Warren, J. D. (2016). The language profile of behavioral variant frontotemporal dementia. Journal of Alzheimer's Disease, 50(2), 359-371. [3] Hillis, A. E., Heidler‐Gary, J., Newhart, M., Chang, S., Ken, L., & Bak, T. H. (2006). Naming and comprehension in primary progressive aphasia: The influence of grammatical word class. Aphasiology, 20(02-04), 246-256. [4] Thompson, C. K., Lukic, S., King, M. C., Mesulam, M. M., & Weintraub, S. (2012). Verb and noun deficits in stroke-induced and primary progressive aphasia: The Northwestern Naming Battery. Aphasiology, 26(5), 632-655.

Keywords: Naming deficits, grammatical categories, neurodegenerative disease, cortical thickness, Temporal and Perisylvian networks

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

Presentation Type: Platform presentation

Topic: Not eligible for student award

Citation: Lukic S, Borghesani V, Shwe W, Weis E, Miller ZA, Deleon J, Neuhaus J, Miller BL and Gorno-Tempini ML (2019). Dissociating Grammatical Categories in Temporal and Perisylvian networks: Evidence from Neurodegenerative Disease. Front. Hum. Neurosci. Conference Abstract: Academy of Aphasia 57th Annual Meeting. doi: 10.3389/conf.fnhum.2019.01.00012

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Received: 29 Apr 2019; Published Online: 09 Oct 2019.

* Correspondence: Dr. Sladjana Lukic, Memory and Aging Center, University of California at San Francisco, San Francisco, California, 94158, United States, Sladjana.lukic@ucsf.edu