Expressive Prosody in Patients With Focal Anterior Temporal Neurodegeneration.

Humans Brain Emotions Empathy Temporal Lobe / diagnostic imaging Cerebral Cortex Frontotemporal Dementia / diagnostic imaging Magnetic Resonance Imaging Aphasia, Primary Progressive / psychology

Journal

Neurology
ISSN: 1526-632X
Titre abrégé: Neurology
Pays: United States
ID NLM: 0401060

Informations de publication

Date de publication:
22 08 2023
Historique:
received: 29 12 2022
accepted: 25 04 2023
pmc-release: 22 08 2024
medline: 23 8 2023
pubmed: 4 7 2023
entrez: 3 7 2023
Statut: ppublish

Résumé

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. 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. 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]; 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.

Sections du résumé

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];
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.

Identifiants

DOI: 10.1212/WNL.0000000000207516 PMID: 37400244 PMC: PMC10449437
pubmed: 37400244
pii: WNL.0000000000207516
doi: 10.1212/WNL.0000000000207516
pmc: PMC10449437
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

e825-e835

Subventions

Organisme : NIA NIH HHS
ID : R01 AG029577
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC016291
Pays : United States
Organisme : NIA NIH HHS
ID : RF1 AG029577
Pays : United States
Organisme : NIA NIH HHS
ID : K08 AG052648
Pays : United States
Organisme : NIA NIH HHS
ID : P50 AG023501
Pays : United States
Organisme : NIA NIH HHS
ID : P01 AG019724
Pays : United States
Organisme : NINDS NIH HHS
ID : RF1 NS050915
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS050915
Pays : United States
Organisme : NIDCD NIH HHS
ID : K24 DC015544
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG038791
Pays : United States
Organisme : NINDS NIH HHS
ID : U54 NS092089
Pays : United States

Informations de copyright

© 2023 American Academy of Neurology.

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Auteurs

Amandine Geraudie (A)

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.

Peter S Pressman (PS)

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.

Jérémie Pariente (J)

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.

Carly Millanski (C)

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.

Eleanor R Palser (ER)

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.

Buddhika M Ratnasiri (BM)

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.

Giovanni Battistella (G)

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.

Maria Luisa Mandelli (ML)

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.

Zachary A Miller (ZA)

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.

Bruce L Miller (BL)

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.

Virginia Sturm (V)

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.

Katherine P Rankin (KP)

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.

Maria Luisa Gorno-Tempini (ML)

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.

Maxime Montembeault (M)

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. maxime.montembeault@mcgill.ca.
ORCID: 0000-0002-9369-0498

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Expressive Prosody in Patients With Focal...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Expressive Prosody in Patients With Focal...
questionsmedicales.fr › Comportement et mécanismes comportementaux › Émotions › Expressive Prosody in Patients With Focal...
questionsmedicales.fr › Comportement et mécanismes comportementaux › Personnalité › Intelligence › Intelligence émotionnelle › Empathie › Expressive Prosody in Patients With Focal...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Télencéphale › Cerveau › Cortex cérébral › Lobe temporal › Expressive Prosody in Patients With Focal...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Télencéphale › Cerveau › Cortex cérébral › Expressive Prosody in Patients With Focal...
questionsmedicales.fr › Troubles mentaux › Troubles neurocognitifs › Démence › Dégénérescence lobaire frontotemporale › Démence frontotemporale › Expressive Prosody in Patients With Focal...
questionsmedicales.fr › Diagnostic › Techniques et procédures diagnostiques › Imagerie diagnostique › Tomographie › Imagerie par résonance magnétique › Expressive Prosody in Patients With Focal...
questionsmedicales.fr › Troubles mentaux › Troubles neurocognitifs › Démence › Aphasie progressive primaire › Expressive Prosody in Patients With Focal...