Differential intrinsic functional connectivity changes in semantic variant primary progressive aphasia

Giovanni Battistella, Maya Henry, Benno Gesierich, Stephen M Wilson, Valentina Borghesani, Wendy Shwe, Zachary Miller, Jessica Deleon, Bruce L. Miller, Jorge Jovicich, Nico Papinutto, Nina F. Dronkers, William W. Seeley, Maria Luisa Mandelli, Maria Luisa Gorno-Tempini

Research output: Contribution to journalArticle

Abstract

The semantic variant of primary progressive aphasia (svPPA) is a clinical syndrome characterized by semantic memory deficits with relatively preserved motor speech, syntax, and phonology. There is consistent evidence linking focal neurodegeneration of the anterior temporal lobes (ATL) to the semantic deficits observed in svPPA. Less is known about large-scale functional connectivity changes in this syndrome, particularly regarding the interplay between affected and spared language networks that leads to the unique cognitive dissociations typical of svPPA. Using whole-brain, seed-based connectivity on task-free Magnetic Resonance Imaging (MRI) data, we studied connectivity of networks anchored to three left-hemisphere regions crucially involved in svPPA symptomatology: ATL just posterior to the main atrophic area, opercular inferior frontal gyrus, and posterior inferior temporal lobe. First, in 32 healthy controls, these seeds isolated three networks: a ventral semantic network involving anterior middle temporal and angular gyri, a dorsal articulatory-phonological system involving inferior frontal and supramarginal regions, and a third functional connection between posterior inferior temporal and intraparietal regions likely involved in linking visual and linguistic processes. We then compared connectivity strength of these three networks between 16 svPPA patients and the 32 controls. In svPPA, decreased functional connectivity in the ventral semantic network correlated with weak semantic skills, while connectivity of the network seeded from the posterior inferior temporal lobe, though not significantly different between the two groups, correlated with pseudoword reading skills. Increased connectivity between the inferior frontal gyrus and the superior portion of the angular gyrus suggested possible adaptive changes. Our findings have two main implications. First, they support a functional subdivision of the left IPL based on its connectivity to specific language-related regions. Second, the unique neuroanatomical and linguistic profile observed in svPPA provides a compelling model for the functional interplay of these networks, being either up- or down- regulated in response to disease.

Original languageEnglish (US)
Article number101797
JournalNeuroImage: Clinical
Volume22
DOIs
StatePublished - Jan 1 2019
Externally publishedYes

Fingerprint

Primary Progressive Aphasia
Semantics
Temporal Lobe
Parietal Lobe
Linguistics
Prefrontal Cortex
Seeds
Language
Dissociative Disorders
Memory Disorders

Keywords

  • Functional connectivity
  • Language
  • Parietal lobe
  • Primary progressive aphasia
  • Resting-state connectivity

ASJC Scopus subject areas

  • Radiology Nuclear Medicine and imaging
  • Neurology
  • Clinical Neurology
  • Cognitive Neuroscience

Cite this

Battistella, G., Henry, M., Gesierich, B., Wilson, S. M., Borghesani, V., Shwe, W., ... Gorno-Tempini, M. L. (2019). Differential intrinsic functional connectivity changes in semantic variant primary progressive aphasia. NeuroImage: Clinical, 22, [101797]. https://doi.org/10.1016/j.nicl.2019.101797

Differential intrinsic functional connectivity changes in semantic variant primary progressive aphasia. / Battistella, Giovanni; Henry, Maya; Gesierich, Benno; Wilson, Stephen M; Borghesani, Valentina; Shwe, Wendy; Miller, Zachary; Deleon, Jessica; Miller, Bruce L.; Jovicich, Jorge; Papinutto, Nico; Dronkers, Nina F.; Seeley, William W.; Mandelli, Maria Luisa; Gorno-Tempini, Maria Luisa.

In: NeuroImage: Clinical, Vol. 22, 101797, 01.01.2019.

Research output: Contribution to journalArticle

Battistella, G, Henry, M, Gesierich, B, Wilson, SM, Borghesani, V, Shwe, W, Miller, Z, Deleon, J, Miller, BL, Jovicich, J, Papinutto, N, Dronkers, NF, Seeley, WW, Mandelli, ML & Gorno-Tempini, ML 2019, 'Differential intrinsic functional connectivity changes in semantic variant primary progressive aphasia', NeuroImage: Clinical, vol. 22, 101797. https://doi.org/10.1016/j.nicl.2019.101797
Battistella, Giovanni ; Henry, Maya ; Gesierich, Benno ; Wilson, Stephen M ; Borghesani, Valentina ; Shwe, Wendy ; Miller, Zachary ; Deleon, Jessica ; Miller, Bruce L. ; Jovicich, Jorge ; Papinutto, Nico ; Dronkers, Nina F. ; Seeley, William W. ; Mandelli, Maria Luisa ; Gorno-Tempini, Maria Luisa. / Differential intrinsic functional connectivity changes in semantic variant primary progressive aphasia. In: NeuroImage: Clinical. 2019 ; Vol. 22.
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AU - Miller, Bruce L.

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