High spatial correlation in brain connectivity between micturition and resting states within bladder-related networks using 7 T MRI in multiple sclerosis women with voiding dysfunction

Zhaoyue Shi, Khue Tran, Christof Karmonik, Timothy Boone, Rose Khavari, Zhaoyue Shi, Khue Tran, Christof Karmonik, Timothy Boone, Rose Khavari

Abstract

Background: Several studies have reported brain activations and functional connectivity (FC) during micturition using functional magnetic resonance imaging (fMRI) and concurrent urodynamics (UDS) testing. However, due to the invasive nature of UDS procedure, non-invasive resting-state fMRI is being explored as a potential alternative. The purpose of this study is to evaluate the feasibility of utilizing resting states as a non-invasive alternative for investigating the bladder-related networks in the brain.

Methods: We quantitatively compared FC in brain regions belonging to the bladder-related network during the following states: 'strong desire to void', 'voiding initiation (or attempt at voiding initiation)', and 'voiding (or continued attempt of voiding)' with FC during rest in nine multiple sclerosis women with voiding dysfunction using fMRI data acquired at 7 T and 3 T.

Results: The inter-subject correlation analysis showed that voiding (or continued attempt of voiding) is achieved through similar network connections in all subjects. The task-based bladder-related network closely resembles the resting-state intrinsic network only during voiding (or continued attempt of voiding) process but not at other states.

Conclusion: Resting states fMRI can be potentially utilized to accurately reflect the voiding (or continued attempt of voiding) network. Concurrent UDS testing is still necessary for studying the effects of strong desire to void and initiation of voiding (or attempt at initiation of voiding).

Keywords: Brain connectivity; Functional magnetic resonance imaging; Multiple sclerosis; Resting states; Urodynamics; Voiding dysfunction.

Conflict of interest statement

The authors declare that they have no conflict of interest.

© 2021. The Author(s).

Figures

Fig. 1
Fig. 1
a Averaged functional connectivity matrices of all 13 ROIs for 9 subjects in the following three urodynamic phases ‘strong desire to void’, ‘initiation of voiding (or attempt at initiation of voiding)’, ‘voiding (or continued attempt of voiding)’, and resting states. The row and column represent each ROI number and their corresponding brain regions can be seen in Table 1. The color bar represents correlation values ranging from -1 to 1. b Group analysis of inter-subject correlations in functional connectivity within 13 ROIs across 9 subjects during three urodynamic phases and resting states, respectively. c The boxplot shows a group analysis of correlations within the bladder-related network between resting states and three urodynamic phases, respectively.

References

    1. Stoffel JT. Contemporary management of the neurogenic bladder for multiple sclerosis patients. Urol Clin North Am. 2010;37(4):547–557. doi: 10.1016/j.ucl.2010.06.003.
    1. Panicker JN, Fowler CJ, Kessler TM. Lower urinary tract dysfunction in the neurological patient: clinical assessment and management. Lancet Neurol. 2015;14(7):720–732. doi: 10.1016/S1474-4422(15)00070-8.
    1. Ogawa S, et al. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A. 1990;87(24):9868–9872. doi: 10.1073/pnas.87.24.9868.
    1. Biswal B, et al. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med. 1995;34(4):537–541. doi: 10.1002/mrm.1910340409.
    1. Chaimow D, et al. Spatial specificity of the functional MRI blood oxygenation response relative to neuronal activity. Neuroimage. 2018;164:32–47. doi: 10.1016/j.neuroimage.2017.08.077.
    1. Shi Z, et al. High spatial correspondence at a columnar level between activation and resting state fMRI signals and local field potentials. Proc Natl Acad Sci U S A. 2017;114(20):5253–5258. doi: 10.1073/pnas.1620520114.
    1. Khavari R, et al. Functional Magnetic Resonance Imaging with Concurrent Urodynamic Testing Identifies Brain Structures Involved in Micturition Cycle in Patients with Multiple Sclerosis. J Urol. 2017;197(2):438–444. doi: 10.1016/j.juro.2016.09.077.
    1. Yin Y, et al. Cerebral activation during withholding urine with full bladder in healthy men using 99mTc-HMPAO SPECT. J Nucl Med. 2006;47(7):1093–1098.
    1. Blok BF, Sturms LM, Holstege G. Brain activation during micturition in women. Brain. 1998;121(Pt 11):2033–2042. doi: 10.1093/brain/121.11.2033.
    1. Seseke S, et al. Voluntary pelvic floor muscle control–an fMRI study. Neuroimage. 2006;31(4):1399–1407. doi: 10.1016/j.neuroimage.2006.02.012.
    1. Shy M, et al. Functional magnetic resonance imaging during urodynamic testing identifies brain structures initiating micturition. J Urol. 2014;192(4):1149–1154. doi: 10.1016/j.juro.2014.04.090.
    1. Schrum A, et al. Motor cortical representation of the pelvic floor muscles. J Urol. 2011;186(1):185–190. doi: 10.1016/j.juro.2011.03.001.
    1. Blok BF, Sturms LM, Holstege G. A PET study on cortical and subcortical control of pelvic floor musculature in women. J Comp Neurol. 1997;389(3):535–544. doi: 10.1002/(SICI)1096-9861(19971222)389:3<535::AID-CNE12>;2-K.
    1. Michels L, et al. Supraspinal Control of Urine Storage and Micturition in Men-An fMRI Study. Cereb Cortex. 2015;25(10):3369–3380. doi: 10.1093/cercor/bhu140.
    1. Zhang H, et al. An fMRI study of the role of suprapontine brain structures in the voluntary voiding control induced by pelvic floor contraction. Neuroimage. 2005;24(1):174–180. doi: 10.1016/j.neuroimage.2004.08.027.
    1. Kuhtz-Buschbeck JP, et al. Cortical representation of the urge to void: A functional magnetic resonance imaging study. J Urol. 2005;174(4):1477–1481. doi: 10.1097/01.ju.0000173007.84102.7c.
    1. Drake MJ, et al. Neural control of the lower urinary and gastrointestinal tracts: supraspinal CNS mechanisms. Neurourol Urodyn. 2010;29(1):119–127. doi: 10.1002/nau.20841.
    1. Sakakibara R. Lower urinary tract dysfunction in patients with brain lesions. Handb Clin Neurol. 2015;130:269–287. doi: 10.1016/B978-0-444-63247-0.00015-8.
    1. Sekido N, Akaza H. Neurogenic bladder may be a side effect of focus resection in an epileptic patient. Int J Urol. 1997;4(1):101–103. doi: 10.1111/j.1442-2042.1997.tb00152.x.
    1. Jang HJ, Kwon MJ, Cho KO. Central Regulation of Micturition and Its Association With Epilepsy. Int Neurourol J. 2018;22(1):2–8. doi: 10.5213/inj.1836040.020.
    1. Blok BF, Willemsen AT, Holstege G. A PET study on brain control of micturition in humans. Brain. 1997;120(Pt 1):111–121. doi: 10.1093/brain/120.1.111.
    1. Harvie C, et al. Brain activation during the voiding phase of micturition in healthy adults: A meta-analysis of neuroimaging studies. Clin Anat. 2019;32(1):13–19. doi: 10.1002/ca.23244.
    1. Alstott J, et al. Modeling the impact of lesions in the human brain. PLoS Comput Biol. 2009;5(6):e1000408. doi: 10.1371/journal.pcbi.1000408.
    1. Griffiths D, et al. Cerebral control of the bladder in normal and urge-incontinent women. Neuroimage. 2007;37(1):1–7. doi: 10.1016/j.neuroimage.2007.04.061.
    1. Tadic SD, et al. Abnormal connections in the supraspinal bladder control network in women with urge urinary incontinence. Neuroimage. 2008;39(4):1647–1653. doi: 10.1016/j.neuroimage.2007.10.059.
    1. Griffiths D. Neural control of micturition in humans: a working model. Nat Rev Urol. 2015;12(12):695–705. doi: 10.1038/nrurol.2015.266.
    1. Shi Z, et al. Realistic models of apparent dynamic changes in resting-state connectivity in somatosensory cortex. Hum Brain Mapp. 2016;37(11):3897–3910. doi: 10.1002/hbm.23284.
    1. Chang C, Glover GH. Time-frequency dynamics of resting-state brain connectivity measured with fMRI. Neuroimage. 2010;50(1):81–98. doi: 10.1016/j.neuroimage.2009.12.011.
    1. Shi Z, et al. On the Relationship between MRI and Local Field Potential Measurements of Spatial and Temporal Variations in Functional Connectivity. Sci Rep. 2019;9(1):8871. doi: 10.1038/s41598-019-45404-8.
    1. Khavari R, et al. Higher neural contribution underlying persistent lower urinary tract symptoms in men with Benign Prostatic Hyperplasia undergoing bladder outlet procedures. Contemp Clin Trials Commun. 2020;17:100498. doi: 10.1016/j.conctc.2019.100498.

Source: PubMed

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