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Research ArticleResearch Article: New Research, Cognition and Behavior

Structural Neuroplasticity Effects of Singing in Chronic Aphasia

Aleksi J. Sihvonen, Anni Pitkäniemi, Sini-Tuuli Siponkoski, Linda Kuusela, Noelia Martínez-Molina, Sari Laitinen, Essi-Reetta Särkämö, Johanna Pekkola, Susanna Melkas, Gottfried Schlaug, Viljami Sairanen and Teppo Särkämö
eNeuro 30 April 2024, 11 (5) ENEURO.0408-23.2024; https://doi.org/10.1523/ENEURO.0408-23.2024
Aleksi J. Sihvonen
1Cognitive Brain Research Unit and Centre of Excellence in Music, Mind, Body and Brain, Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, Helsinki 00014, Finland
2School of Health and Rehabilitation Sciences, Queensland Aphasia Research Centre and UQ Centre for Clinical Research, The University of Queensland, Brisbane QLD 4072, Australia
3Department of Neurology, University of Helsinki and Helsinki University Hospital, Helsinki 00029, Finland
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  • ORCID record for Aleksi J. Sihvonen
Anni Pitkäniemi
1Cognitive Brain Research Unit and Centre of Excellence in Music, Mind, Body and Brain, Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, Helsinki 00014, Finland
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Sini-Tuuli Siponkoski
1Cognitive Brain Research Unit and Centre of Excellence in Music, Mind, Body and Brain, Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, Helsinki 00014, Finland
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Linda Kuusela
4HUS Helsinki Medical Imaging Center, Helsinki University Hospital, Helsinki 00029, Finland
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Noelia Martínez-Molina
1Cognitive Brain Research Unit and Centre of Excellence in Music, Mind, Body and Brain, Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, Helsinki 00014, Finland
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Sari Laitinen
5Espoo Hospital, Espoo 00029, Finland
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Essi-Reetta Särkämö
6Private Choir Conductor, Vantaa 01520, Finland
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Johanna Pekkola
4HUS Helsinki Medical Imaging Center, Helsinki University Hospital, Helsinki 00029, Finland
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Susanna Melkas
3Department of Neurology, University of Helsinki and Helsinki University Hospital, Helsinki 00029, Finland
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Gottfried Schlaug
7Department of Neurology, UMass Medical School, Springfield, Massachusetts 01655
8Department of Biomedical Engineering and Institute of Applied Life Sciences, UMass Amherst, Amherst, Massachusetts 01655
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Viljami Sairanen
4HUS Helsinki Medical Imaging Center, Helsinki University Hospital, Helsinki 00029, Finland
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Teppo Särkämö
1Cognitive Brain Research Unit and Centre of Excellence in Music, Mind, Body and Brain, Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, Helsinki 00014, Finland
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Article Figures & Data

Figures

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  • Figure 1.
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    Figure 1.

    Flowchart.

  • Figure 2.
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    Figure 2.

    Lesion overlap map of all patients (N = 28). The n-value represents the number of patients with a lesion to a specific voxel.

  • Figure 3.
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    Figure 3.

    Treatment-induced WM neuroplasticity changes. Connectometry results displaying the significant segments of the tracts with longitudinal QA increases significantly associated with singing group versus control group between T1 and T2 (ΔT2–T1; left) and longitudinal QA change correlation with improved naming (right). FDR, false discovery rate; L, left; QA, quantitative anisotropy; R, right.

  • Figure 4.
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    Figure 4.

    Treatment-induced GM neuroplasticity changes. Longitudinal GM volume increases (singing group > control group) in T2 > T1 and longitudinal GM volume change correlation with improved naming. Additional exploratory voxel-wise analyses are reported in Extended Data Figure 4-1. Bar plots for mean group GM volume changes are shown: bar, mean; error bar, standard error of mean. BA, Brodmann area; FDR, false discovery rate; vPMC, ventral premotor cortex.

Tables

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    Table 1.

    Demographic and clinical characteristics of the patients

    AllSinging groupControl groupp-value
    N = 28N = 13N = 15
    Demographical
     Age (years)64.7 (8.4)64.1 (8.8)65.2 (8.3)0.731 (t)
     Sex (male/female)14/147/67/80.705 (χ2)
     Handedness (right/left)23/512/111/40.191 (χ2)
     Education levela3.0 (1.3)3.2 (1.4)2.9 (1.3)0.492 (U)
    Music background
     Choir singing years3.3 (9.3)3.8 (12.4)2.8 (6.0)0.389 (U)
     Singing lessons years0.6 (3.5)0.0 (0.0)1.2 (4.6)0.352 (U)
     Instrument lessons years0.8 (2.3)0.2 (0.6)1.3 (3.0)0.325 (U)
    Clinical
     Time from injury (months)78.1 (82.0)69.7 (77.9)85.4 (87.3)0.982 (U)
     Lesion size (cm3)89.3 (85.3)119.0 (75.6)63.5 (87.1)0.023 (U)
     Type of stroke (ischemic/hemorrhagic)20/811/29/60.150 (χ2)
     AQ score (mild or moderate/severe)b20/88/512/30.281 (χ2)
     BDAE verbal agility score7.7 (4.8)6.5 (5.2)8.8 (4.2)0.339 (U)
    Received rehabilitation (T1–T2)
     Speech therapyc7.3 (10.8)7.6 (11.6)6.9 (10.4)0.717 (U)
     Physical therapyc6.9 (12.3)8.5 (15.7)5.5 (8.8)1.000 (U)
     Occupational therapyc2.2 (5.7)3.9 (8.0)0.7 (1.5)0.525 (U)
     Neuropsychological rehabilitationc0.3 (1.2)0.0 (0.0)0.6 (1.6)0.555 (U)
    • Data are mean (SD) unless otherwise reported. Bold values denote statistical significance at p < 0.05. t, t test; χ2, chi-square test; U, Mann–Whitney U test; AQ, aphasia quotient; BDAE, Boston Diagnostic Aphasia Examination.

    • ↵a Education level according to the UNESCO International Standard Classification of Education: range 1 (primary education) to 6 (doctoral or equivalent level).

    • ↵b Aphasia severity based on the AQ score: 0–50 = severe, 51–100 = mild/moderate.

    • ↵c Data are mean (SD) in hours between T1 and T2.

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    Table 2.

    Spoken language and neuroplasticity analysis outcomes

    MeasureGroupT1 mean (SD)T2 mean (SD)ΔT2 > T1 mean (SD)Baseline diff. (pFDR-value)ΔT2 > T1 (pFDR-value)
    Spoken language outcomes
     WAB NamingSinging5.0 (3.6)5.7 (3.8)0.7 (0.7)0.5850.006
    Control7.4 (3.6)7.4 (3.5)0.0 (0.5)
     WAB RepetitionSinging5.4 (3.6)5.7 (3.4)0.3 (0.7)0.5850.277
    Control7.6 (3.4)7.6 (3.3)0.0 (0.4)
    Neuroplasticity outcomes
     GMV left BA44aSinging747 (568)807 (586)61 (108)0.9450.008
    Control854 (387)713 (427)−140 (141)
     GMV right BA44aSinging1,619 (159)1,628 (278)9 (99)0.7180.587
    Control1,798 (336)1,743 (324)−55 (149)
     GMV left BA45aSinging387 (304)414 (306)28 (43)0.9450.024
    Control409 (240)336 (263)−73 (78)
     GMV right BA45aSinging873 (159)891 (173)19 (61)0.7200.759
    Control924 (201)913 (164)−11 (110)
     GMV left vPMCaSinging884 (567)941 (607)57 (203)0.7180.024
    Control1,106 (400)913 (460)−195 (151)
     GMV right vPMCaSinging1,783 (293)1,775 (309)−8 (105)0.8330.876
    Control1,827 (448)1,810 (370)−21 (172)
     GMV left pMTGaSinging1,103 (718)1,090 (724)−13 (76)0.7180.268
    Control1,383 (430)1,431 (591)47 (56)
     GMV right pMTGaSinging2,205 (533)2,242 (551)37 (137)0.7180.777
    Control2,498 (503)2,513 (477)14 (74)
     WM left AFbSinging0.10 (0.04)0.11 (0.05)0.01 (0.01)0.4800.005
    Control0.11 (0.04)0.11 (0.05)0.00 (0.02)
     WM left FATbSinging0.13 (0.03)0.14 (0.04)0.01 (0.02)0.5230.004
    Control0.14 (0.05)0.13 (0.06)−0.01 (0.02)
     WM right FATbSinging0.19 (0.03)0.20 (0.03)0.01 (0.01)0.8150.004
    Control0.20 (0.03)0.19 (0.02)0.00 (0.02)
     WM left SLFbSinging0.10 (0.05)0.11 (0.05)0.01 (0.01)0.4800.005
    Control0.11 (0.04)0.11 (0.05)0.00 (0.02)
     WM right SLFbSinging0.21 (0.03)0.22 (0.03)0.01 (0.01)0.4800.004
    Control0.20 (0.03)0.20 (0.03)0.00 (0.01)
     WM left CSbSinging0.09 (0.04)0.10 (0.04)0.01 (0.01)0.4800.004
    Control0.10 (0.04)0.10 (0.05)0.00 (0.01)
     WM right CSbSinging0.16 (0.04)0.17 (0.04)0.01 (0.01)0.5550.004
    Control0.17 (0.03)0.17 (0.02)0.00 (0.01)
     WM CCbSinging0.14 (0.03)0.15 (0.03)0.01 (0.01)0.4800.005
    Control0.15 (0.03)0.15 (0.03)−0.01 (0.01)
    • Data are mean (SD) unless otherwise reported. Bold values denote statistical significance at p < 0.05. P-values are FDR corrected.

    • ↵a Volume in mm3.

    • ↵b Normalized QA.

Extended Data

  • Figures
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  • Figure 4-1

    Voxel-wise analysis of the treatment-induced grey matter neuroplasticity changes. Longitudinal GM volume increases (Singing group>Control Group) in T2>T1 from (left) the whole-brain voxel-wise analysis, (middle) the voxel-wise analysis within the language network derived from meta-analysis (https://neurosynth.org/analyses/terms/language/) and (right) the voxel-wise analysis within the study-specific regions of interest. BA=Brodmann area, FWE=Family-wise error rate, vPMC=ventral premotor cortex. Download Figure 4-1, TIF file.

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Structural Neuroplasticity Effects of Singing in Chronic Aphasia
Aleksi J. Sihvonen, Anni Pitkäniemi, Sini-Tuuli Siponkoski, Linda Kuusela, Noelia Martínez-Molina, Sari Laitinen, Essi-Reetta Särkämö, Johanna Pekkola, Susanna Melkas, Gottfried Schlaug, Viljami Sairanen, Teppo Särkämö
eNeuro 30 April 2024, 11 (5) ENEURO.0408-23.2024; DOI: 10.1523/ENEURO.0408-23.2024

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Structural Neuroplasticity Effects of Singing in Chronic Aphasia
Aleksi J. Sihvonen, Anni Pitkäniemi, Sini-Tuuli Siponkoski, Linda Kuusela, Noelia Martínez-Molina, Sari Laitinen, Essi-Reetta Särkämö, Johanna Pekkola, Susanna Melkas, Gottfried Schlaug, Viljami Sairanen, Teppo Särkämö
eNeuro 30 April 2024, 11 (5) ENEURO.0408-23.2024; DOI: 10.1523/ENEURO.0408-23.2024
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Keywords

  • aphasia
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