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Articles, Behavioral/Systems/Cognitive

Brain Activity during Ankle Proprioceptive Stimulation Predicts Balance Performance in Young and Older Adults

Daniel J. Goble, James P. Coxon, Annouchka Van Impe, Monique Geurts, Michail Doumas, Nicole Wenderoth and Stephan P. Swinnen
Journal of Neuroscience 9 November 2011, 31 (45) 16344-16352; DOI: https://doi.org/10.1523/JNEUROSCI.4159-11.2011
Daniel J. Goble
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James P. Coxon
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Annouchka Van Impe
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Monique Geurts
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Michail Doumas
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Nicole Wenderoth
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Stephan P. Swinnen
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  • Figure 1.
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    Figure 1.

    Clusters of neural activity (p < 0.05 FWE cluster corrected) rendered on a standard T1 template for vibrotactile stimulation (i.e., BONE > REST) of the left (red) and right (blue) lower limbs of young and older adults. S1, Primary somatosensory cortex; SMG, supramarginal gyrus; Post Ins, posterior insula.

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    Figure 2.

    Clusters of neural activity (p < 0.05 FWE cluster corrected) rendered on standard T1 template for muscle spindle stimulation (i.e., TENDON > BONE) of the left (red), right (blue), and both (green) feet of young and older adults. IFG, Inferior frontal gyrus; Ant Ins, anterior insula; BG, basal ganglia; OFC, orbital frontal cortex; DLPFC, dorsolateral prefrontal cortex; SMG, supramarginal gyrus; IPC, inferior parietal cortex; PMv, premotor ventral region; S1, primary somatosensory cortex; M1, primary motor cortex.

  • Figure 3.
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    Figure 3.

    Left, Largest cluster (green, rendered on standard MNI template) of voxels showing a significant positive correlation (FDR < 0.01) between neural activity during TENDON > BONE (i.e., muscle spindle) stimulation and balance performance (i.e., ES). Right, Clusterwise PSC for YOUNG (red) and OLD (yellow) averaged across feet correlated with ES; r values are used as a measure of strength of relationship. OFC, Orbital frontal cortex; Ant Ins, anterior insula; IFG p. tri, inferior frontal gyrus pars triangularis; IFG p. oper, inferior frontal gyrus pars opercularis; BG, basal ganglia.

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    Figure 4.

    Top, Second through fourth largest clusters (green, rendered on standard MNI templates at top) of voxels showing significant positive correlation (FDR < 0.01) between neural activity during TENDON > BONE (i.e., muscle spindle) stimulation and balance performance (i.e., ES). Bottom, Cross-plots of the relationship between clusterwise PSC averaged across feet and balance performance in YOUNG (red) and OLD (yellow), r values indicate strength of relation. Ant Ins, Anterior insula; SMG, supramarginal gyrus; IPC, inferior parietal cortex.

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    Figure 5.

    Fifth through eighth largest clusters (green, rendered on standard MNI templates) of voxels showing significant positive correlation (FDR < 0.01) between neural activity during TENDON > BONE (i.e., muscle spindle) stimulation and balance performance (i.e., ES). Next to each render, the relationship between clusterwise PSC averaged across feet and balance performance in YOUNG (red) and OLD (yellow) is cross-plotted with r values to indicate strength of relation. PMv, Premotor ventral; S2, secondary somatosensory; DLPFC, dorsolateral prefrontal cortex.

Tables

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    Table 1.

    List of clusters showing significant muscle spindle-related brain activity

    TENDON > BONE peak locationSidexyzt value
    Cluster 1: 4205 voxels
        Inferior frontal gyrus (p. tri, BA 45)R5416−25.78
        Inferior frontal gyrus (p. oper, BA 44)R5216164.97
        Anterior insular lobe (BA 48)R2820−85.63
        Precentral gyrus (PMv, BA 6)R5010385.44
    R484464.73
    R506484.73
        Orbitofrontal cortex (BA 47)R4422−145.07
    R4842−44.15
        Basal ganglia (pallidum)R18004.8
    R22024.75
        Basal ganglia (putamen)R3410−44.74
        ThalamusR14−804.49
    Cluster 2: 2142 voxels
        Supramarginal gyrus (BA 40)R60−42426.10
        Supramarginal gyrus (BA 40/2)R64−38406.08
    R64−34305.57
        Inferior parietal cortex (BA 40)R60−44485.88
    Cluster 3: 2123 voxels
        Inferior frontal gyrus (p. oper, BA 44)L−5010125.31
    L−501244.96
        Anterior insular lobeL−302045.2
    L−3220−64.94
    L−3418−84.94
        Inferior frontal gyrus (p. tri, BA 45)L−4816−25.2
        Basal ganglia (putamen)L−24084.38
    L−26264.35
        Basal ganglia (pallidum)L−16223.79
        ThalamusL−20−684.14
    Cluster 4: 1809 voxels
        Pre-SMA (BA 6)R814585.49
    R810605.44
    L−102704.18
    L−410583.97
        SMA (BA 6)R10−4704.71
    R2−20724.22
    L−10−4784.33
    L−14−6704.18
    L−10−12744.09
    L−6−6643.85
        Dorsal anterior cingulate (BA 32)R622485.27
    R826344.61
    Cluster 5: 938 voxels
        Inferior parietal cortex (BA 40)L−62−48405.31
    L−60−48444.95
    L−58−44504.81
    L−56−46524.4
    L−60−58343.65
        Supramarginal gyrus (BA 40/2)L−64−44364.81
    L−66−36324.04
    L−60−30463.93
        Supramarginal gyrus (BA 2)L−56−24304.37
    L−56−28304.36
    Cluster 6: 422 voxels
        Middle frontal gyrus (DLPFC, BA 46)R2850204.49
    R3840344.23
    • R, Right; L, left; p. tri, pars triangularis; p. oper, pars opercularis; PMv, premotor ventral; DLPFC, dorsolateral prefrontal cortex.

    • View popup
    Table 2.

    Summary of mean (±SE) sway metrics for younger and older adults with p values from t test measuring YOUNG > OLD performance

    Sway parameterYoungerOlderp value
    Max AP excursion (ES)93.1 (±0.4)91.8 (±0.5)<0.05
    Max ML excursion (cm)0.60 (±0.04)0.67 (±0.05)0.16
    RMS AP (cm)0.34 (±0.02)0.4 (±0.1)0.10
    RMS ML (cm)0.11 (±0.01)0.13 (±0.01)0.09
    AP velocity (cm/s)25.3 (±0.6)29.1 (±1.8)<0.05
    ML velocity (cm/s)18.9 (±0.4)20.2 (±0.8)0.07
    • View popup
    Table 3.

    List of brain areas showing significant association between muscle spindle-related brain activity (i.e. TENDON > BONE) and balance performance in terms of ES

    Location of peak association with ESSidexyzt valuep value
    Cluster 1: 2148 voxels
        Anterior insulaR362084.830.004
    R303023.490.004
    R3026−23.470.004
        Inferior frontal gyrus (p. tri, BA 45)R384484.620.004
    R364444.530.004
        Orbital frontal cortex (BA 47)R5022−144.440.004
        Inferior frontal gyrus (p. oper, BA 44)R486144.370.004
    R54423.960.004
        Basal ganglia (putamen)R20−6103.310.005
        Basal ganglia (pallidum)R22−883.260.005
    Cluster 2: 528 voxels
        pre-SMA (BA 6)R818684.130.004
    R82703.720.004
    R822583.450.004
    R216483.190.006
        Dorsal anterior cingulate (BA 32)R824422.970.008
    R628402.960.008
    Cluster 3: 404 voxels
        Anterior insulaL−302804.250.004
    L−361603.720.004
    L−2620−83.380.005
    Cluster 4: 347 voxels
        Supramarginal gyrus (BA 40)R56−36443.630.004
    R54−36403.620.004
    Cluster 5: 232 voxels
        Middle frontal gyrus (DLPFC, BA 46)R3246164.220.004
    R2650223.900.004
    Cluster 6: 131 voxels
        Middle frontal gyrus (DLPFC, BA 9)R4818443.370.004
    R4814423.150.006
        Precentral gyrus (BA 6)R426363.300.005
    R4610443.170.006
    R4612403.160.006
    R524403.020.008
    Cluster 7: 41 voxels
        Middle frontal gyrus (DLPFC, BA 46)R3830323.710.004
    R3638342.990.008
    Cluster 8: 37 voxels
        Parietal operculum (S2, BA 43)R68−20203.730.004
    • R, Right; L, left; p. tri, pars triangularis; p. oper, pars opercularis; DLPFC, dorsolateral prefrontal cortex; S2, secondary somatosensory region.

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The Journal of Neuroscience: 31 (45)
Journal of Neuroscience
Vol. 31, Issue 45
9 Nov 2011
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Brain Activity during Ankle Proprioceptive Stimulation Predicts Balance Performance in Young and Older Adults
Daniel J. Goble, James P. Coxon, Annouchka Van Impe, Monique Geurts, Michail Doumas, Nicole Wenderoth, Stephan P. Swinnen
Journal of Neuroscience 9 November 2011, 31 (45) 16344-16352; DOI: 10.1523/JNEUROSCI.4159-11.2011

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Brain Activity during Ankle Proprioceptive Stimulation Predicts Balance Performance in Young and Older Adults
Daniel J. Goble, James P. Coxon, Annouchka Van Impe, Monique Geurts, Michail Doumas, Nicole Wenderoth, Stephan P. Swinnen
Journal of Neuroscience 9 November 2011, 31 (45) 16344-16352; DOI: 10.1523/JNEUROSCI.4159-11.2011
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