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March 10, 2020; 94 (10) Article

Right hemisphere ventral stream for emotional prosody identification

Evidence from acute stroke

View ORCID ProfileShannon M. Sheppard, Lynsey M. Keator, Bonnie L. Breining, Amy E. Wright, Sadhvi Saxena, Donna C. Tippett, Argye E. Hillis
First published December 31, 2019, DOI: https://doi.org/10.1212/WNL.0000000000008870
Shannon M. Sheppard
From the Departments of Neurology (S.M.S., L.M.K., B.L.B., A.E.W., S.S., D.C.T., A.E.H.), Physical Medicine and Rehabilitation (D.C.T., A.E.H.), and Otolaryngology–Head and Neck Surgery (D.C.T.), Johns Hopkins University School of Medicine; and Department of Cognitive Science (A.E.H.), Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD.
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  • ORCID record for Shannon M. Sheppard
Lynsey M. Keator
From the Departments of Neurology (S.M.S., L.M.K., B.L.B., A.E.W., S.S., D.C.T., A.E.H.), Physical Medicine and Rehabilitation (D.C.T., A.E.H.), and Otolaryngology–Head and Neck Surgery (D.C.T.), Johns Hopkins University School of Medicine; and Department of Cognitive Science (A.E.H.), Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD.
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Bonnie L. Breining
From the Departments of Neurology (S.M.S., L.M.K., B.L.B., A.E.W., S.S., D.C.T., A.E.H.), Physical Medicine and Rehabilitation (D.C.T., A.E.H.), and Otolaryngology–Head and Neck Surgery (D.C.T.), Johns Hopkins University School of Medicine; and Department of Cognitive Science (A.E.H.), Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD.
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Amy E. Wright
From the Departments of Neurology (S.M.S., L.M.K., B.L.B., A.E.W., S.S., D.C.T., A.E.H.), Physical Medicine and Rehabilitation (D.C.T., A.E.H.), and Otolaryngology–Head and Neck Surgery (D.C.T.), Johns Hopkins University School of Medicine; and Department of Cognitive Science (A.E.H.), Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD.
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Sadhvi Saxena
From the Departments of Neurology (S.M.S., L.M.K., B.L.B., A.E.W., S.S., D.C.T., A.E.H.), Physical Medicine and Rehabilitation (D.C.T., A.E.H.), and Otolaryngology–Head and Neck Surgery (D.C.T.), Johns Hopkins University School of Medicine; and Department of Cognitive Science (A.E.H.), Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD.
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Donna C. Tippett
From the Departments of Neurology (S.M.S., L.M.K., B.L.B., A.E.W., S.S., D.C.T., A.E.H.), Physical Medicine and Rehabilitation (D.C.T., A.E.H.), and Otolaryngology–Head and Neck Surgery (D.C.T.), Johns Hopkins University School of Medicine; and Department of Cognitive Science (A.E.H.), Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD.
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Argye E. Hillis
From the Departments of Neurology (S.M.S., L.M.K., B.L.B., A.E.W., S.S., D.C.T., A.E.H.), Physical Medicine and Rehabilitation (D.C.T., A.E.H.), and Otolaryngology–Head and Neck Surgery (D.C.T.), Johns Hopkins University School of Medicine; and Department of Cognitive Science (A.E.H.), Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD.
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Citation
Right hemisphere ventral stream for emotional prosody identification
Evidence from acute stroke
Shannon M. Sheppard, Lynsey M. Keator, Bonnie L. Breining, Amy E. Wright, Sadhvi Saxena, Donna C. Tippett, Argye E. Hillis
Neurology Mar 2020, 94 (10) e1013-e1020; DOI: 10.1212/WNL.0000000000008870

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Abstract

Objective To determine whether right ventral stream and limbic structures (including posterior superior temporal gyrus [STG], STG, temporal pole, inferior frontal gyrus pars orbitalis, orbitofrontal cortex, amygdala, anterior cingulate, gyrus, and the sagittal stratum) are implicated in emotional prosody identification.

Methods Patients with MRI scans within 48 hours of unilateral right hemisphere ischemic stroke were enrolled. Participants were presented with 24 sentences with neutral semantic content spoken with happy, sad, angry, afraid, surprised, or bored prosody and chose which emotion the speaker was feeling based on tone of voice. Multivariable linear regression was used to identify individual predictors of emotional prosody identification accuracy from a model, including percent damage to proposed right hemisphere structures, age, education, and lesion volume across all emotions (overall emotion identification) and 6 individual emotions. Patterns of recovery were also examined at the chronic stage.

Results The overall emotion identification model was significant (adjusted r2 = 0.52; p = 0.043); greater damage to right posterior STG (p = 0.038) and older age (p = 0.009) were individual predictors of impairment. The model for recognition of fear was also significant (adjusted r2 = 0.77; p = 0.002), with greater damage to right amygdala (p = 0.047), older age (p < 0.001), and less education (p = 0.005) as individual predictors. Over half of patients with chronic stroke had residual impairments.

Conclusions Right posterior STG in the right hemisphere ventral stream is critical for emotion identification in speech. Patients with stroke with damage to this area should be assessed for emotion identification impairment.

Glossary

DWI=
diffusion-weighted imaging;
IFG=
inferior frontal gyrus;
OFC=
orbitofrontal cortex;
RH=
right hemisphere;
STG=
superior temporal gyrus;
STS=
superior temporal sulcus

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.

  • Received December 24, 2018.
  • Accepted in final form September 4, 2019.
  • © 2019 American Academy of Neurology
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