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August 22, 2023; 101 (8) Research Article

Expressive Prosody in Patients With Focal Anterior Temporal Neurodegeneration

Amandine Geraudie, Peter S. Pressman, Jérémie Pariente, Carly Millanski, Eleanor R. Palser, Buddhika M. Ratnasiri, Giovanni Battistella, Maria Luisa Mandelli, Zachary A. Miller, Bruce L. Miller, Virginia Sturm, Katherine P. Rankin, Maria Luisa Gorno-Tempini, View ORCID ProfileMaxime Montembeault
First published July 3, 2023, DOI: https://doi.org/10.1212/WNL.0000000000207516
Amandine Geraudie
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Peter S. Pressman
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Jérémie Pariente
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Carly Millanski
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Eleanor R. Palser
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Buddhika M. Ratnasiri
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Giovanni Battistella
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Maria Luisa Mandelli
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Zachary A. Miller
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Bruce L. Miller
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Virginia Sturm
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Katherine P. Rankin
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Maria Luisa Gorno-Tempini
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Maxime Montembeault
From the Memory and Aging Center (A.G., E.R.P., B.M.R., G.B., M.L.M., Z.A.M., B.L.M., V.S., K.P.R., M.L.G.-T., M.M.), Department of Neurology, University of California San Francisco; Neurology Department (A.G., J.P.), Toulouse University Hospital; Institut du Cerveau (ICM) (A.G.), INSERM U1127, CNRS UMR 7225, Sorbonne Université, Paris, France; Department of Neurology (P.S.P.), University of Colorado; Department of Speech (C.M.), Language, and Hearing Sciences, The University of Texas at Austin; Dyslexia Center (E.R.P., M.L.M., Z.A.M., V.S., M.L.G.-T.), Department of Neurology, University of California San Francisco; Department of Otolaryngology—Head and Neck Surgery (G.B.), Massachusets Eye and Ear and Harvard Medical School, Boston; Douglas Research Centre (M.M.); and Department of Psychiatry (M.M.), McGill University, Montréal, Quebec, Canada.
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Expressive Prosody in Patients With Focal Anterior Temporal Neurodegeneration
Amandine Geraudie, Peter S. Pressman, Jérémie Pariente, Carly Millanski, Eleanor R. Palser, Buddhika M. Ratnasiri, Giovanni Battistella, Maria Luisa Mandelli, Zachary A. Miller, Bruce L. Miller, Virginia Sturm, Katherine P. Rankin, Maria Luisa Gorno-Tempini, Maxime Montembeault
Neurology Aug 2023, 101 (8) e825-e835; DOI: 10.1212/WNL.0000000000207516

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Abstract

Background and Objectives Progressive focal anterior temporal lobe (ATL) neurodegeneration has been historically called semantic dementia. More recently, semantic variant primary progressive aphasia (svPPA) and semantic behavioral variant frontotemporal dementia (sbvFTD) have been linked with predominant left and right ATL neurodegeneration, respectively. Nonetheless, clinical tools for an accurate diagnosis of sbvFTD are still lacking. Expressive prosody refers to the modulation of pitch, loudness, tempo, and quality of voice used to convey emotional and linguistic information and has been linked to bilateral but right-predominant frontotemporal functioning. Changes in expressive prosody can be detected with semiautomated methods and could represent a useful diagnostic marker of socioemotional functioning in sbvFTD.

Methods Participants underwent a comprehensive neuropsychological and language evaluation and a 3T MRI at the University of California San Francisco. Each participant provided a verbal description of the picnic scene from the Western Aphasia Battery. The fundamental frequency (f0) range, an acoustic measure of pitch variability, was extracted for each participant. We compared the f0 range between groups and investigated associations with an informant-rated measure of empathy, a facial emotion labeling task, and gray matter (GM) volumes using voxel-based morphometry.

Results Twenty-eight patients with svPPA, 18 with sbvFTD, and 18 healthy controls (HCs) were included. f0 range was significantly different across groups: patients with sbvFTD showed reduced f0 range in comparison with both patients with svPPA (mean difference of −1.4 ± 2.4 semitones; 95% CI −2.4 to −0.4]; p < 0.005) and HCs (mean difference of −1.9 ± 3.0 semitones; 95% CI −3.0 to −0.7]; p < 0.001). A higher f0 range was correlated with a greater informant-rated empathy (r = 0.355; p ≤ 0.05), but not facial emotion labeling. Finally, the lower f0 range was correlated with lower GM volume in the right superior temporal gyrus, encompassing anterior and posterior portions (p < 0.05 FWE cluster corrected).

Discussion Expressive prosody may be a useful clinical marker of sbvFTD. Reduced empathy is a core symptom in sbvFTD; the present results extend this to prosody, a core component of social interaction, at the intersection of speech and emotion. They also inform the long-standing debate on the lateralization of expressive prosody in the brain, highlighting the critical role of the right superior temporal lobe.

Glossary

ATL=
anterior temporal lobe;
CATS=
Comprehensive Affect Testing System;
CDR=
Clinical Dementia Rating Scale;
GM=
gray matter;
HCs=
healthy controls;
MAC=
Memory and Aging Center;
MMSE=
Mini-Mental State Examination;
nfvPPA=
nonfluent/agrammatic variant of primary progressive aphasia;
RSMS=
Revised Self-Monitoring Scale;
sbvFTD=
semantic behavioral variant frontotemporal dementia;
SD=
semantic dementia;
svPPA=
semantic variant primary progressive aphasia;
UCSF=
University of California San Francisco;
VBM=
voxel-based morphometry

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Submitted and externally peer reviewed. The handling editors were Assistant Editor Andrea Schneider, MD, PhD and Deputy Editor Bradford Worrall, MD, MSc, FAAN.

  • Received December 29, 2022.
  • Accepted in final form April 25, 2023.
  • © 2023 American Academy of Neurology
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