Clinical Practice
Examining mechanisms of brain control of bladder function with resting state functional connectivity MRI†,‡
Rahel Nardos,
William Thomas Gregory,
Christine Krisky,
Amanda Newell,
Binyam Nardos, Bradley Schlaggar, Damien A. Fair,
Corresponding Author
Rahel Nardos
Oregon Health and Science University, Portland, Oregon
Kaiser Permanente, Clackamas, Oregon
Correspondence to: Rahel Nardos, Mail Code: L466, 3181 S.W. Sam Jackson Park Rd., Portland, OR 97239-3107. E-mail: [email protected]Search for more papers by this authorWilliam Thomas Gregory
Oregon Health and Science University, Portland, Oregon
Search for more papers by this authorChristine Krisky
Oregon Health and Science University, Portland, Oregon
Search for more papers by this authorAmanda Newell
Oregon Health and Science University, Portland, Oregon
Search for more papers by this authorDamien A. Fair
Oregon Health and Science University, Portland, Oregon
Search for more papers by this authorRahel Nardos,
William Thomas Gregory,
Christine Krisky,
Amanda Newell,
Binyam Nardos, Bradley Schlaggar, Damien A. Fair,
Corresponding Author
Rahel Nardos
Oregon Health and Science University, Portland, Oregon
Kaiser Permanente, Clackamas, Oregon
Correspondence to: Rahel Nardos, Mail Code: L466, 3181 S.W. Sam Jackson Park Rd., Portland, OR 97239-3107. E-mail: [email protected]Search for more papers by this authorWilliam Thomas Gregory
Oregon Health and Science University, Portland, Oregon
Search for more papers by this authorChristine Krisky
Oregon Health and Science University, Portland, Oregon
Search for more papers by this authorAmanda Newell
Oregon Health and Science University, Portland, Oregon
Search for more papers by this authorDamien A. Fair
Oregon Health and Science University, Portland, Oregon
Search for more papers by this author†
Dirk De Ridder led the peer-review process as the Associate Editor responsible for the paper.
‡
Conflict of interest: none.
Abstract
Aims
This aim of this study is to identify the brain mechanisms involved in bladder control.
Methods
We used fMRI to identify brain regions that are activated during bladder filling. We then used resting state connectivity fMRI (rs-fcMRI) to assess functional connectivity of regions identified by fMRI with the rest of the brain as the bladder is filled to capacity.
Results
Female participants (n = 20) were between ages 40 and 64 with no significant history of symptomatic urinary incontinence. Main effect of time (MET) fMRI analysis resulted in 20 regions of interest (ROIs) that have significant change in BOLD signal (z = 3.25, P <0.05) over the course of subtle bladder filling and emptying regardless of full versus empty bladder state. Bladder-state by time (BST) fMRI analysis resulted in three ROIs that have significant change in BOLD signal (z = 3.25, P <0.05) over the course of bladder runs comparing full versus empty bladder state. Rs-fcMRI fixed effects analysis identified significant changes in connectivity between full and empty bladder states in seven brain regions (z = 4.0) using the three BST ROIs and sixteen brain regions (z = 7) using the twenty MET ROIs. Regions identified include medial frontal gyrus, posterior cingulate (PCC), inferiolateral temporal and post-central gyrus, amygdale, the caudate, inferior parietal lobe as well as anterior and middle cingulate gyrus.
Conclusions
There is significant and vast changes in the brain's functional connectivity when bladder is filled suggesting that the central process responsible for the increased control during the full bladder state appears to largely rely on the how distributed brain systems are functionally integrated. Neurourol. Urodynam. 33:493–501, 2014. © 2013 Wiley Periodicals, Inc.
REFERENCES
- 1 Stewart WF, Van Rooyen JB, Cundiff GW, et al. Prevalence and burden of overactive bladder in the United States. World J Urol 2003; 20: 327–36.
- 2 Norton P, Brubaker L. Urinary incontinence in women. Lancet 2006; 367: 57–67.
- 3 Coyne KS, Sexton CC, Kopp ZS, et al. The impact of overactive bladder on mental health, work productivity and health-related quality of life in the UK and Sweden: Results from EpiLUTS. BJU Int 2011; 108: 1459–71.
- 4 Brubaker L. Urgency: The cornerstone symptom of overactive bladder. Urology 2004; 64: 12–6.
- 5 Martin JL, Williams KS, Sutton AJ, et al. Systematic review and meta-analysis of methods of diagnostic assessment for urinary incontinence. Neurourol Urodyn 2006; 25: 674–83; discussion 684.
- 6 Athwal BS, Berkley KJ, Hussain I, et al. Brain responses to changes in bladder volume and urge to void in healthy men. Brain 2001; 124: 369–77.
- 7
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: 535–44.
10.1002/(SICI)1096-9861(19971222)389:3<535::AID-CNE12>3.0.CO;2-K CAS PubMed Web of Science® Google Scholar
- 8 Griffiths D, Derbyshire S, Stenger A, et al. Brain control of normal and overactive bladder. J Urol 2005 174: 1862–7.
- 9 Nour S, Svarer C, Kristensen JK, et al. Cerebral activation during micturition in normal men. Brain 2000; 123: 781–9.
- 10 Zhang H, Reitz A, Kollias S, 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: 174–80.
- 11 Griffiths D, Tadic SD. Bladder control, urgency, and urge incontinence: Evidence from functional brain imaging. Neurourol Urodyn 2008 27: 466–74.
- 12 Griffiths D, Tadic SD, Schaefer W, et al. Cerebral control of the bladder in normal and urge-incontinent women. Neuroimage 2007; 37: 1–7.
- 13 Logothetis NK. What we can do and what we cannot do with fMRI. Nature 2008; 453: 869–78.
- 14 Biswal B, Yetkin FZ, Haughton VM, et al. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 1995; 34: 537–41.
- 15 Fair DA, Dosenbach NU, Church JA, et al. Development of distinct control networks through segregation and integration. Proc Natl Acad Sci USA 2007; 104: 13507–12.
- 16 Nir Y, Hasson U, Levy I, et al. Widespread functional connectivity and fMRI fluctuations in human visual cortex in the absence of visual stimulation. Neuroimage 2006; 30: 1313–24.
- 17 Greicius MD, Krasnow B, Reiss AL, et al. Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 2003; 100: 253–8.
- 18 Fox MD, Raichle ME. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 2007; 8: 700–11.
- 19 Salvador R, Suckling J, Coleman MR, et al. Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb Cortex 2005; 15: 1332–42.
- 20 Achard S, Salvador R, Whitcher B, et al. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci 2006; 26: 63–72.
- 21 Damoiseaux JS, Rombouts SA, Barkhof F, et al. Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 2006; 103: 13848–53.
- 22 Dosenbach NU, Fair DA, Miezin FM, et al. Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci USA 2007; 104: 11073–8.
- 23 Fair DA, Schlaggar BL, Cohen AL, et al. A method for using blocked and event-related fMRI data to study “resting state” functional connectivity. Neuroimage 2007; 35: 396–405.
- 24 Avery K, Donovan J, Peters TJ, et al. ICIQ: A brief and robust measure for evaluating the symptoms and impact of urinary incontinence. Neurourol Urodyn 2004; 23: 322–30.
- 25 Barber MD, Walters MD, Bump RC. Short forms of two condition-specific quality-of-life questionnaires for women with pelvic floor disorders (PFDI-20 and PFIQ-7). Am J Obstet Gynecol 2005; 193: 103–13.
- 26 Miezin FM, Maccotta L, Ollinger JM, et al. Characterizing the hemodynamic response: Effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. Neuroimage 2000; 6: 735–59.
- 27 Fox MD, Snyder AZ, Vincent JL, et al. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 2005; 102: 9673–8.
- 28 Fair DA, Cohen AL, Dosenbach NU, et al. The maturing architecture of the brain's default network. Proc Natl Acad Sci USA 2008; 105: 4028–32.
- 29 Fair DA, Snyder AZ, Connor LT, et al. Task-evoked BOLD responses are normal in areas of diaschisis after stroke. Neurorehabil Neural Repair 2009; 23: 52–7.
- 30 Power JD, Cohen AL, Nelson SM, et al. Functional network organization of the human brain. Neuron 2011; 72: 665–78.
- 31 Power JD, Barnes KA, Snyder AZ, et al. Spurious but systematic correlations in functional connectivity MRI networks arise from Subject motion. NeuroImage 2012; 59: 2142–54.
- 32 Brown TT, Lugar HM, Coalson RS, et al. Developmental changes in human cerebral functional organization for word generation. Cereb Cortex 2005; 15: 275–90.
- 33 Fair DA, Brown TT, Petersen SE, et al. A comparison of analysis of variance and correlation methods for investigating cognitive development with functional magnetic resonance imaging. Dev Neuropsychol 2006; 30: 531–46.
- 34 Schlaggar BL, Brown TT, Lugar HM, et al. Functional neuroanatomical differences between adults and school-age children in the processing of single words. Science 2002; 296: 1476–9.
- 35 Fair DA, Brown TT, Petersen SE, et al. fMRI reveals novel functional neuroanatomy in a child with perinatal stroke. Neurology 2006; 67: 2246–9.
- 36 Van Essen DC. A population-average, landmark- and surface-based (PALS) atlas of human cerebral cortex. Neuroimage 2005; 28: 635–62.
- 37 Van Essen DC, Drury HA, Dickson J, et al. An integrated software suite for surface-based analyses of cerebral cortex. J Am Med Inform Assoc 2001; 8: 443–59.
- 38 Lancaster JL, Woldorff MG, Parsons LM, et al. Automated Talairach atlas labels for functional brain mapping. Human Brain Mapping 2000; 10: 120–31.
- 39 Craig AD. Interoception: The sense of the physiological condition of the body. Curr Opin Neurobiol 2003; 13: 500–5.
- 40 Fowler CJ, Griffiths DJ. A decade of functional brain imaging applied to bladder control. Neurourol Urodyn 2010; 29: 49–55.
- 41 Critchley HD, Wiens S, Rotshtein P, et al. Neural systems supporting interoceptive awareness. Nat Neurosci 2004; 7: 189–95.
- 42 MacDonald AW, III, Cohen JD, Stenger VA, et al. Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 2000; 288: 1835–8.
- 43 Shulman GL, Fiez JA, Corbetta M, et al. Common blood flow changes across visual tasks:II; decreases in cerebral cortex. J Cogn Neurosci 1997; 9: 648–63.
- 44 Raichle ME, MacLeod AM, Snyder AZ, et al. A default mode of brain function. Proc Natl Acad Sci USA 2001; 98: 676–82.
- 45 Raichle ME, Snyder AZ. A default mode of brain function: A brief history of an evolving idea. Neuroimage 2007; 37: 1083–90; discussion 1097–9.
- 46 Seseke S, Baudewig J, Kallenberg K, et al. Voluntary pelvic floor muscle control—An fMRI study. Neuroimage 2006; 31: 1399–407.
- 47 Dosenbach NU, Visscher KM, Palmer ED, et al. A core system for the implementation of task sets. Neuron 2006; 50: 799–812.
- 48 Wolf U, Rapoport MJ, Schweizer TA. Evaluating the affective component of the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci 2009; 21: 245–53.
- 49 Kuhtz-Buschbeck JP, van der Horst C, Pott C, et al. Cortical representation of the urge to void: A functional magnetic resonance imaging study. J Urol 2005; 174: 1477–81.
- 50 Pontari MA, Mohamed FB, Lebovitch S, et al. Central nervous system findings on functional magnetic resonance imaging in patients before and after treatment with anticholinergic medication. J Urol 2010; 183: 1899–905.
- 51 Andrews-Hanna JR. The brain's default network and its adaptive role in internal mentation. Neuroscientist 2012; 18: 251–70.
- 52 Buckner RL, Andrews-Hanna JR, Schacter DL. The brain's default network: Anatomy, function, and relevance to disease. Ann N Y Acad Sci 2008; 1124: 1–38.
- 53 Tagliazucchi E, Balenzuela P, Fraiman D, et al. Brain resting state is disrupted in chronic back pain patients. Neurosci Lett 2010; 485: 26–31.
- 54 Bluhm RL, Miller J, Lanius RA, et al. Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: Anomalies in the default network. Schizophr Bull 2007; 33: 1004–12.
- 55 Wu X, Li R, Fleisher AS, et al. Altered default mode network connectivity in Alzeimer's disease—A resting functional MRI and Bayesean Network Study. Hum Brain Mapp 2011; 0: 1–14.
- 56 Fair DA, Posner J, Nagel BJ, et al. Atypical default network connectivity in youth with attention-deficit/hyperactivity disorder. Biol Psychiatry 2010; 68: 1084–91.
- 57 Yamamoto T, Sakakibara R, Hashimoto K, et al. Striatal dopamine level increases in the urinary storage phase in cats: An in vivo microdialysis study. Neuroscience 2005; 135: 299–303.
- 58 Sakakibara R, Nakazawa K, Uchiyama T, et al. Effects of subthalamic nucleus stimulation on the micturation reflex in cats. Neuroscience 2003; 120: 871–5.
- 59 Fowler CJ, Dalton C, Panicker JN. Review of neurologic diseases for the urologist. Urol Clin North Am 2010; 37: 517–26.
- 60 Morris JS, Frith CD, Perrett DI, et al. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 1996; 383: 812–5.
- 61 Blok BF, Groen J, Bosch JL, et al. Different brain effects during chronic and acute sacral neuromodulation in urge incontinent patients with implanted neurostimulators. BJU Int 2006; 98: 1238–43.
- 62 Binkofski F, Schnitzler A, Enck P, et al. Somatic and limbic cortex activation in esophageal distention: A functional magnetic resonance imaging study. Ann Neurol 1998; 44: 811–5.
- 63 Hobday DI, Aziz Q, Thacker N, et al. A study of the cortical processing of ano-rectal sensation using functional MRI. Brain 2001; 124: 361–8.
- 64 Jafri MJ, Pearlson GD, Stevens M, et al. A method for functional network connectivity among spatially independent resting-state components in schizophrenia. Neuroimage 2008; 39: 1666–81.
- 65 Li SJ, Li Z, Wu G, et al. Alzheimer disease: Evaluation of a functional MR imaging index as a marker. Radiology 2002; 225: 253–9.
Citing Literature
