Spared speech fluency is associated with increased functional connectivity in the speech production network in semantic variant primary progressive aphasia

Maxime Montembeault; Zachary A Miller; Amandine Geraudie; Peter Pressman; Antoine Slegers; Carly Millanski; Abigail Licata; Buddhika Ratnasiri; Maria Luisa Mandelli; Maya Henry; Yann Cobigo; Howard J Rosen; Bruce L Miller; Simona M Brambati; Maria Luisa Gorno-Tempini; Giovanni Battistella

doi:10.1093/braincomms/fcad077

Spared speech fluency is associated with increased functional connectivity in the speech production network in semantic variant primary progressive aphasia

Brain Commun. 2023 Mar 16;5(2):fcad077. doi: 10.1093/braincomms/fcad077. eCollection 2023.

Authors

Maxime Montembeault^{1

2

3}, Zachary A Miller¹, Amandine Geraudie^{1

4}, Peter Pressman⁵, Antoine Slegers^{6

7}, Carly Millanski^{1

8}, Abigail Licata¹, Buddhika Ratnasiri¹, Maria Luisa Mandelli¹, Maya Henry⁸, Yann Cobigo¹, Howard J Rosen¹, Bruce L Miller¹, Simona M Brambati^{6

7}, Maria Luisa Gorno-Tempini¹, Giovanni Battistella^{1

9}

Affiliations

¹ Memory and Aging Center, Department of Neurology, University of California in San Francisco, San Francisco, CA 94158, USA.
² Douglas Mental Health University Institute, Montréal, QC H4H 1R3, Canada.
³ Department of Psychiatry, McGill University, Montréal, QC H3A 1A1, Canada.
⁴ Department of Neurology, Toulouse University Hospital, Toulouse 31400, France.
⁵ Department of Neurology, Behavioral Neurology Section, University of Colorado Anschutz Medical Campus, Aurora, CO 80238, USA.
⁶ Département de Psychologie, Université de Montréal, Montréal, QC H3C 3J7, Canada.
⁷ Centre de recherche de l'Institut Universitaire de Gériatrie de Montréal, Montréal, QC H3W 1W5, Canada.
⁸ Department of Speech, Language, and Hearing Sciences, The University of Texas at Austin, Austin, TX 78712-0114, USA.
⁹ Department of Otolaryngology-Head and Neck Surgery, Massachusetts Eye and Ear and Harvard Medical School, Boston, MA 02114, USA.

Abstract

Semantic variant primary progressive aphasia is a clinical syndrome characterized by marked semantic deficits, anterior temporal lobe atrophy and reduced connectivity within a distributed set of regions belonging to the functional network associated with semantic processing. However, to fully depict the clinical signature of semantic variant primary progressive aphasia, it is necessary to also characterize preserved neural networks and linguistic abilities, such as those subserving speech production. In this case-control observational study, we employed whole-brain seed-based connectivity on task-free MRI data of 32 semantic variant primary progressive aphasia patients and 46 healthy controls to investigate the functional connectivity of the speech production network and its relationship with the underlying grey matter. We investigated brain-behaviour correlations with speech fluency measures collected through clinical tests (verbal agility) and connected speech (speech rate and articulation rate). As a control network, we also investigated functional connectivity within the affected semantic network. Patients presented with increased connectivity in the speech production network between left inferior frontal and supramarginal regions, independent of underlying grey matter volume. In semantic variant primary progressive aphasia patients, preserved (verbal agility) and increased (articulation rate) speech fluency measures correlated with increased connectivity between inferior frontal and supramarginal regions. As expected, patients demonstrated decreased functional connectivity in the semantic network (dependent on the underlying grey matter atrophy) associated with average nouns' age of acquisition during connected speech. Collectively, these results provide a compelling model for studying compensation mechanisms in response to disease that might inform the design of future rehabilitation strategies in semantic variant primary progressive aphasia.

Keywords: compensation mechanism; functional connectivity; semantic variant of primary progressive aphasia; semantics; speech production.

Abstract

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