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Articles, Behavioral/Cognitive

Neural Basis of Acquired Amusia and Its Recovery after Stroke

Aleksi J. Sihvonen, Pablo Ripollés, Vera Leo, Antoni Rodríguez-Fornells, Seppo Soinila and Teppo Särkämö
Journal of Neuroscience 24 August 2016, 36 (34) 8872-8881; DOI: https://doi.org/10.1523/JNEUROSCI.0709-16.2016
Aleksi J. Sihvonen
1Faculty of Medicine, University of Turku, 20520 Turku, Finland,
2Cognitive Brain Research Unit, Institute of Behavioural Sciences, University of Helsinki, 00014 Helsinki, Finland,
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Pablo Ripollés
3Cognition and Brain Plasticity Group, Bellvitge Biomedical Research Institute, L'Hospitalet de Llobregat, 08907 Barcelona, Spain,
4Department of Basic Psychology, University of Barcelona, 08035 Barcelona, Spain, and
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Vera Leo
2Cognitive Brain Research Unit, Institute of Behavioural Sciences, University of Helsinki, 00014 Helsinki, Finland,
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Antoni Rodríguez-Fornells
3Cognition and Brain Plasticity Group, Bellvitge Biomedical Research Institute, L'Hospitalet de Llobregat, 08907 Barcelona, Spain,
4Department of Basic Psychology, University of Barcelona, 08035 Barcelona, Spain, and
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Seppo Soinila
5Division of Clinical Neurosciences, Turku University Hospital and Department of Neurology, University of Turku, 20521, Turku, Finland
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Teppo Särkämö
2Cognitive Brain Research Unit, Institute of Behavioural Sciences, University of Helsinki, 00014 Helsinki, Finland,
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  • Figure 1.
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    Figure 1.

    Lesion-overlap maps for all subjects. A, Lesion distribution for the whole sample. Warmer areas indicate areas of greater lesion overlap. Accordingly, the color scale ranges from 2 to 26 overlapping subjects. B, Statistical power map for VLSM analyses with 77 patients. The map is thresholded at Z > 4 to view lesion areas with sufficient statistical power to detect an effect of Z ≥ 4.

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    Figure 2.

    VLSM results for amusia and aphasia. A, MBEA Scale and Rhythm average score (%). B, BDAE-ASRS score. C, Amusic versus NA patients. D, Aphasic versus nonaphasic patients. Amusia is based on MBEA Scale and Rhythm average score (cutoff, 75%) and aphasia is based on BDAE-ASRS (cutoff, <5). N = 77. Neurological convention is used with MNI coordinates at the bottom left of each slice. All statistical maps are thresholded at a FDR-corrected p < 0.05 threshold. INS, Insula; PUT, putamen.

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    Figure 3.

    Binary lesion analyses with pure amusics and pure aphasics. A–D, Comparisons between A, amusic versus NA patients (all aphasic patients excluded; N = 47); B, aphasic versus nonaphasic patients (all amusic patients excluded; N = 28); C, amusic versus aphasic and amusic patients (N = 49); and D, amusic (no aphasia) versus aphasic (no amusia; N = 40). Amusia is based on MBEA Scale and Rhythm average score (cutoff, 75%) and aphasia is based on BDAE-ASRS (cutoff, <5). Neurological convention is used with MNI coordinates at the bottom left of each slice. All statistical maps are thresholded at a FDR-corrected p < 0.05 threshold. INS, Insula; PUT, putamen.

  • Figure 4.
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    Figure 4.

    VLSM results for scale and rhythm amusia. A, MBEA Scale score. B, MBEA Rhythm score. C, An overlap image comparing Rhythm (red) and Scale (blue) subtests' parametric results (N = 77). Neurological convention is used with MNI coordinates at the bottom left of each slice. All statistical maps are thresholded at a FDR-corrected p < 0.05 threshold. GP, Globus pallidum; PUT, putamen.

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    Figure 5.

    VBM results of 47 Helsinki patients. Time (Acute >6 months) × Group (NRAs > NAs) in GMV or WMV interaction. A, GM NRAs (N = 16) versus NAs (N = 18). B, GM (hot) and WM (cold) nonrecovered rhythm amusics (N = 11) versus nonrhythm amusics (N = 18). C, GM nonrecovered pitch amusics (N = 13) versus nonpitch amusics (N = 17). Bar plots for GMV differences in Acute >6 months. Bar, mean; error bar, SEM. The results are reported at an uncorrected p < 0.001 threshold at the voxel level (extent threshold: k > 50 voxels) using MNI coordinates. Clusters for analysis A and B pass a p < 0.05 FWE-corrected threshold at the cluster level.

Tables

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    Table 1.

    Demographic and clinical characteristics of the patients

    VLSM analysis (n = 77) of Helsinki and Turku patientsVBM analysis (n = 47) of Helsinki patients
    Amusic (n = 49)NA (n = 28)p valueNRA (n = 16)RA (n = 13)NA (n = 18)p value
    Demographic
        Gender (male/female)26/2317/110.51 (χ2)6/107/612/60.24 (χ2)
        Age (years)59.9 (10.6)55.8 (10.3)0.09 (t)62.2 (7.7)58.5 (5.4)56.6 (9.9)0.13 (F)
        Education (years)10.6 (3.7)13.6 (3.1)<0.001 (t)9.6 (2.6)9.8 (4.2)13.2 (3.1)0.003 (F)
    Music background (prestroke)
        Formal music traininga0.04 (0.29)0.11 (0.58)0.65 (U)0.00 (0.00)0.00 (0.00)0.19 (0.68)0.19 (K)
        Instrument playinga1.10 (1.70)1.96 (2.25)0.11 (U)1.46 (1.86)1.26 (1.94)1.30 (1.81)0.90 (K)
        Music listening prior to strokeb4.8 (2.0)3.8 (1.8)0.96 (U)3.3 (1.8)3.4 (1.4)3.9 (1.1)0.61 (K)
    Clinical
        Aphasia (no/yes)c29/2017/110.89 (χ2)10/610/311/70.61 (χ2)
        BDAE-ASRS4.3 (1.1)4.4 (0.9)0.51 (U)4.3 (1.1)4.5 (1.1)4.3 (1.1)0.89 (K)
        MBEA total score percentage58.0 (8.6)84.3 (6.2)<0.001 (t)57.8 (10.5)55.2 (8.8)84.9 (7.1)<0.001 (F)
        MBEA Rhythm score percentage58.1 (12.0)82.0 (8.9)<0.001 (t)60.3 (13.8)56.0 (12.3)84.1 (9.7)<0.001 (F)
        MBEA Scale score percentage57.8 (12.3)86.6 (8.4)<0.001 (t)55.5 (12.6)54.4 (8.5)85.7 (9.2)<0.001 (F)
        Visual neglect (no/yes)d26/1828/0<0.001 (χ2)9/77/618/00.004 (χ2)
        Other cognitive dysfunction (no/yes)e2/474/240.11 (χ2)0/161/122/160.41 (χ2)
        Hemiparesis (no/yes)11/388/200.55 (χ2)4/122/114/140.81 (χ2)
        Lesion laterality (left/right)18/3116/120.08 (χ2)8/83/1010/80.17 (χ2)
        Lesion volume in cm355.8 (43.7)25.5 (27.8)0.001 (t)57.6 (46.4)49.2 (35.9)25.3 (31.7)0.04 (F)
    • Data are mean (SD) unless otherwise stated. χ2, χ2 Test; F, one-way ANOVA; K, Kruskal–Wallis test; t, t test; U, Mann–Whitney U test.

    • ↵aNumbers denote values on a Likert scale: 0, no; 1, <1 year; 2, 1–3 years; 3, 4–6 years; 4, 7–10 years; 5, >10 years of training/playing.

    • ↵bNumbers denote values on a Likert scale: range, 0 (never does) to 5 (does daily).

    • ↵cClassification based on BDAE ASRS: scores 0–4, aphasia; score 5, no aphasia.

    • ↵dClassification based on the Lateralized Inattention Index of the Balloons Test.

    • ↵eOther cognitive dysfunction (attention/executive function or memory deficit).

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    Table 2.

    Anatomical correlates of VLSM results for MBEA Scale and Rhythm scores

    Anatomical regionScaleRhythm
    Right caudate90.02%94.86%
    Right HG**40.58%90.53%
    Right insula*38.56%59.23%
    Right pallidum86.82%89.81%
    Right putamen90.02%94.86%
    Right MTG**1.97%18.55%
    Right STG**11.25%57.04%
    Right middle temporal pole0.70%1.98%
    Right superior temporal pole2.70%6.33%
    • The lesion patterns associated with poor performance in MBEA Scale and Rhythm subtests were overlaid with anatomical masks created with the WFU PickAtlas to obtain the amount of damaged voxels in different anatomical regions. For visual results, see Figure 4.

    • ↵*p < 0.05, **p < 0.005; comparison (χ2) between the percentages of damaged voxels in Rhythm versus Scale (i.e., if the damaged area within the structure is larger in Rhythm than in Scale).

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    Table 3.

    GMV and WMV decreases (6 month–acute)

    Anatomical areaMNI coordinatesCluster sizet value
    GM NRAs versus NAs
        Right MTG (BA 21)54 −33 −384434.20*
        Right STG (BA 22)53 −35 −4
        Right inferior temporal gyrus (BA 37)58 −62 −6
    GM and WM nonrecovered rhythm amusics versus nonrhythm amusics
        Right STG (BA 38)47 17 −41158664.85*
        Right middle temporal pole53 17 −32; 65 0 −9
        Right MTG WM50 −24 −1439314.66*
        Right IFG WM49 −8 −26; 49 −17 −18
    GM nonrecovered pitch amusics versus nonpitch amusics
        Right MTG (BA 21)63 −62 67903.76**
        Right MTG (BA 19)61 −69 12; 63 −64 −6
    • For visual VBM results, see Figure 5. IFG, Inferior Temporal Gyrus.

    • ↵*p < 0.05 FWE-corrected at the cluster level.

    • ↵**p < 0.01 uncorrected at the cluster level

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The Journal of Neuroscience: 36 (34)
Journal of Neuroscience
Vol. 36, Issue 34
24 Aug 2016
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Neural Basis of Acquired Amusia and Its Recovery after Stroke
Aleksi J. Sihvonen, Pablo Ripollés, Vera Leo, Antoni Rodríguez-Fornells, Seppo Soinila, Teppo Särkämö
Journal of Neuroscience 24 August 2016, 36 (34) 8872-8881; DOI: 10.1523/JNEUROSCI.0709-16.2016

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Neural Basis of Acquired Amusia and Its Recovery after Stroke
Aleksi J. Sihvonen, Pablo Ripollés, Vera Leo, Antoni Rodríguez-Fornells, Seppo Soinila, Teppo Särkämö
Journal of Neuroscience 24 August 2016, 36 (34) 8872-8881; DOI: 10.1523/JNEUROSCI.0709-16.2016
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Keywords

  • amusia
  • aphasia
  • music
  • stroke
  • voxel-based lesion-symptom mapping
  • voxel-based morphometry

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