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Articles, Behavioral/Cognitive

Cortical Activation Associated with Muscle Synergies of the Human Male Pelvic Floor

Skulpan Asavasopon, Manku Rana, Daniel J. Kirages, Moheb S. Yani, Beth E. Fisher, Darryl H. Hwang, Everett B. Lohman, Lee S. Berk and Jason J. Kutch
Journal of Neuroscience 8 October 2014, 34 (41) 13811-13818; DOI: https://doi.org/10.1523/JNEUROSCI.2073-14.2014
Skulpan Asavasopon
1Physical Therapy Department, Loma Linda University, Loma Linda, California 92350,
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Manku Rana
2Division of Biokinesiology and Physical Therapy and
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Daniel J. Kirages
2Division of Biokinesiology and Physical Therapy and
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Moheb S. Yani
2Division of Biokinesiology and Physical Therapy and
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Beth E. Fisher
2Division of Biokinesiology and Physical Therapy and
5Department of Neurology, University of Southern California, Los Angeles, California 90033
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Darryl H. Hwang
3Department of Radiology, University of Southern California, Los Angeles, California 90033,
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Everett B. Lohman
1Physical Therapy Department, Loma Linda University, Loma Linda, California 92350,
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Lee S. Berk
1Physical Therapy Department, Loma Linda University, Loma Linda, California 92350,
4Department of Pathology and Human Anatomy, Loma Linda University, Loma Linda, California 92350, and
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Jason J. Kutch
2Division of Biokinesiology and Physical Therapy and
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  • Figure 1.
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    Figure 1.

    EMG evidence of pelvic floor muscle synergies. A, EMG signals from the PFM (blue), GMM (green), and the FDI (red) were recorded during separate trials that focused on the voluntary activation of each of these muscle groups. B, Example EMG recordings from the PFM and GMM muscles in a single participant during repeated voluntary PFM activation and separate voluntary GMM activation. Participants performed two blocks of 10 activations, each activation lasting 2 s. We observed PFM muscle activation during voluntary GMM muscle activation, but no GMM muscle activation during voluntary PFM muscle activation. C, Group data demonstrating the consistent finding of synergistic activation of the PFM muscles during voluntary GMM muscle activation but not during voluntary FDI muscle activation. Moreover, we did not find evidence of FDI or GMM muscle activation during voluntary PFM muscle activation. Curves show the average EMG transient triggered by the onset of the primary voluntary muscle of the task, averaged across participants (error bars indicate SEM across participants). D, Statistical analysis of group data shows that PFM activity is significantly greater (*p < 0.01) during voluntary GMM activation compared with PFM activity during voluntary FDI activation. The activity in the primary muscles of the tasks (GMM and FDI) was not significantly different (p = 0.40, n.s.; error bars indicate SEM across participants). E, Analysis of the normalized EMG transients for the PFM and GMM muscles during voluntary GMM muscle activation revealed that activation of PFM muscles led GMM muscle activation by an average of 128 ms across participants (minimum of 30.5 ms and maximum of 239.5 ms; p = 0.001).

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    Figure 2.

    fMRI evidence of overlapping activity during voluntary PFM and voluntary GMM activation. A, fMRI data were collected while participants performed three separate runs identical to the EMG tasks: separate repeated voluntary activation of PFM (run 1), GMM (run 2), and FDI (run 3). B, Contrast of voluntary FDI activation greater than voluntary PFM activation produced significant brain activation in left sensorimotor cortex. C, Contrast of voluntary PFM activation greater than voluntary FDI activation produced significant activation in the medial wall of the precentral gyrus. D, Contrast of voluntary GMM activation greater than voluntary FDI activation produced significant activation in the medial wall of the precentral gyrus E, Anterior medial wall of the precentral gyrus exhibited significant brain activation for both PFM activation and GMM activation compared with FDI activation.

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    Figure 3.

    TMS evidence that region of brain activation overlap between voluntary PFM activation and voluntary GMM activation is associated with the activity in PFM muscles. A, We collected MEP from the PFM muscles generated by TMS along the midline of the participant's brain. B, Single participant data showing an MEP in the PFM muscles generated by stimulating over precentral gyrus at a latency of 23 ms. Stimulating at points not over the precentral gyrus did not generate significant MEPs. The MEP in the PFM peaked at an MNI coordinate at approximately −20 mm. C, Locations of applied stimulation across all participants confined over the midline and divided (binned) into posterior, middle (precentral gyrus), and anterior bins. D, ANOVA analysis revealed that bin location had a significant main effect on MEP magnitude (*p = 0.003). MEPs corresponding to the middle bin were significantly greater than either the posterior bin (p = 0.001) or anterior bin (p = 0.016). Error bars indicate SEM across participants. E, Stimulation points classified as precentral gyrus were above the fMRI-identified region of activation common to both voluntary PFM activation and voluntary GMM activation.

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    Figure 4.

    Evidence of motor cortical representation in the overlapping brain activation during voluntary PFM and voluntary GMM activation. We computed the number of voxels in the overlap that were most likely to belong to each of the 121 regions in the Jülich Histological Atlas within FSL. The range of atlas regions included in each BA are labeled. CST, Corticospinal tract.

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    Table 1.

    Peak foci for activation in the region of overlap obtained during voluntary PFM and voluntary GMM activation

    RegionPFM > FDIGMM > FDI
    Coordinates x, y, z (mm)Z scoreCoordinates x, y, z (mm)Z score
    Primary motor cortex (4)20, −32, 644.7018, −30, 684.86
    Premotor cortex (SMA, 6)−4, −20, 663.16−4, −22, 643.82
    Primary somatosensory cortex (1–3)−16, −34, 663.7416, −36, 644.67
    Superior parietal lobule (5)−6, −40, 482.9810, −40, 544.07
    • Significance: Z > 2.3, p < 0.05, cluster-corrected for multiple comparisons. Coordinates in standard MNI space.

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The Journal of Neuroscience: 34 (41)
Journal of Neuroscience
Vol. 34, Issue 41
8 Oct 2014
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Cortical Activation Associated with Muscle Synergies of the Human Male Pelvic Floor
Skulpan Asavasopon, Manku Rana, Daniel J. Kirages, Moheb S. Yani, Beth E. Fisher, Darryl H. Hwang, Everett B. Lohman, Lee S. Berk, Jason J. Kutch
Journal of Neuroscience 8 October 2014, 34 (41) 13811-13818; DOI: 10.1523/JNEUROSCI.2073-14.2014

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Cortical Activation Associated with Muscle Synergies of the Human Male Pelvic Floor
Skulpan Asavasopon, Manku Rana, Daniel J. Kirages, Moheb S. Yani, Beth E. Fisher, Darryl H. Hwang, Everett B. Lohman, Lee S. Berk, Jason J. Kutch
Journal of Neuroscience 8 October 2014, 34 (41) 13811-13818; DOI: 10.1523/JNEUROSCI.2073-14.2014
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Keywords

  • EMG
  • fMRI
  • motor cortex
  • pelvic floor
  • supplementary motor area
  • TMS

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