Voluntary pelvic floor muscle control—an fMRI study

Storage and periodic expulsion of urine by the bladder are controlled by central pathways and organized as simple on-off switching circuits. Several reports concerning aspects of micturition control have identified distinct regions in the brainstem, like the pontine micturition center (PMC) and the periaqueductal gray (PAG), as well as the cerebellum, basal ganglia, limbic system, and cortical areas that are organized in a widespread network. The present study focused on the involvement of these specific brain regions in pelvic floor muscle control. Functional magnetic resonance imaging (fMRI) was performed at 3T in 11 healthy women with urge to void due to a filled bladder, who were instructed to either imitate voiding by releasing or to imitate interruption of voiding by contracting pelvic floor muscles. None of the subjects was able to start voiding during the experiments, presumably due to subconscious restraint resulting from the inconvenient situation. Relaxation and contraction of pelvic floor muscles induced strong and similar activation patterns including frontal cortex, sensory-motor cortex, cerebellum, and basal ganglia. Furthermore, well-localized activations in the PMC and the PAG were identified. To our knowledge, this is the first study using fMRI to demonstrate micturition-related activity in these brainstem structures. The presented approach proved to characterize the widespread central network in pelvic floor muscle control. Thus, in patients with voiding dysfunction, fMRI will be useful to elucidate the individual disturbance level.

[1]  Carlo Caltagirone,et al.  Effects of subthalamic nucleus stimulation on urodynamic findings in patients with Parkinson's disease. , 2003, The Journal of urology.

[2]  H. Fukuyama,et al.  Neural control of micturition in man examined with single photon emission computed tomography using 99mTc‐HMPAO , 1996, Neuroreport.

[3]  H. Saito,et al.  Mesial frontal lobe syndromes: correlations between neurological deficits and radiological localizations. , 1990, The Tohoku journal of experimental medicine.

[4]  William C. de Groat,et al.  Anatomy of the central neural pathways controlling the lower urinary tract. , 1998 .

[5]  D C Good,et al.  Causes of Urinary Incontinence After Acute Hemispheric Stroke , 1993, Stroke.

[6]  G. Holstege,et al.  The neuronal control of micturition and its relation to the emotional motor system. , 1996, Progress in brain research.

[7]  G. Holstege,et al.  Brain activation during micturition in women. , 1998, Brain : a journal of neurology.

[8]  T. Ruch,et al.  Localization of brain stem and diencephalic areas controlling the micturation reflex , 1956, The Journal of comparative neurology.

[9]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[10]  G. Holstege,et al.  Anatomical and physiological observations on suprapinal control of bladder and urethral sphincter muscles in the cat , 1986, The Journal of comparative neurology.

[11]  S. Matsuura,et al.  Human brain region response to distention or cold stimulation of the bladder: a positron emission tomography study. , 2002, The Journal of urology.

[12]  D. Griffiths Clinical studies of cerebral and urinary tract function in elderly people with urinary incontinence , 1998, Behavioural Brain Research.

[13]  G. Holstege,et al.  Ultrastructural evidence for a paucity of projections from the lumbosacral cord to the pontine micturition center or M‐region in the cat: A new concept for the organization of the micturition reflex with the periaqueductal gray as central relay , 1995, The Journal of comparative neurology.

[14]  G. Holstege,et al.  A PET study on brain control of micturition in humans. , 1997, Brain : a journal of neurology.

[15]  S. Siegel,et al.  Selecting patients for sacral nerve stimulation. , 2005, The Urologic clinics of North America.

[16]  H. Noto,et al.  Effect of cerebellectomy on reflex micturition in the decerebrate dog as determined by urodynamic evaluation. , 1989, Urologia internationalis.

[17]  B. Schmitz,et al.  Lateralization in autononic dysfunction in ischemic stroke involving the insular cortex , 2004, Neuroreport.

[18]  J Andrew,et al.  The Cerebral Control of Micturition , 1965, Proceedings of the Royal Society of Medicine.

[19]  Armin Curt,et al.  An fMRI study of the role of suprapontine brain structures in the voluntary voiding control induced by pelvic floor contraction , 2005, NeuroImage.

[20]  R Gjone,et al.  Excitatory and inhibitory bladder responses to stimulation of 'limbic', diencephalic and mesencephalic structures in the cat. , 1966, Acta physiologica Scandinavica.

[21]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[22]  C. J. Fowler,et al.  Voiding and MRI Analysis of the Brain , 1999, International Urogynecology Journal.

[23]  Y. Kuroiwa,et al.  Frequency and urgency of micturition in hemiplegic patients: relationship to hemisphere laterality of lesions , 1987, Journal of Neurology.

[24]  M. Kuru,et al.  Fiber connections of the pontine detrusor nucleus (Barrington) , 1964, The Journal of comparative neurology.

[25]  Komei Ueki,et al.  DISTURBANCES OF MICTURITION OBSERVED IN SOME PATIENTS WITH BRAIN TUMOR , 1960 .

[26]  Pazo Jh Caudate-putamen and globus pallidus influences on a visceral reflex. , 1976 .

[27]  Robert W. Blair,et al.  Responses of neurons in ventroposterolateral nucleus of primate thalamus to urinary bladder distension , 1992, Brain Research.

[28]  J. Girvin,et al.  Cardiovascular effects of human insular cortex stimulation , 1992, Neurology.

[29]  A Sundin,et al.  Identification of human brain loci processing esophageal sensation using positron emission tomography. , 1997, Gastroenterology.

[30]  Richard S. J. Frackowiak,et al.  Brain responses to changes in bladder volume and urge to void in healthy men. , 2001, Brain : a journal of neurology.

[31]  W. Penfield The Cerebral Cortex of Man , 1950 .

[32]  G. Holstege,et al.  A PET study on cortical and subcortical control of pelvic floor musculature in women , 1997, The Journal of comparative neurology.

[33]  C. Fowler,et al.  Neurological disorders of micturition and their treatment. , 1999, Brain : a journal of neurology.

[34]  I. Tracey,et al.  Cortical Processing of Human Somatic and Visceral Sensation , 1999, The Journal of Neuroscience.

[35]  Gert Holstege,et al.  Control and coordination of bladder and urethral function in the brainstem of the cat , 1990 .

[36]  F. Barrington,et al.  THE EFFECT OF LESIONS OF THE HIND‐ AND MID‐BRAIN ON MICTURITION IN THE CAT , 1925 .

[37]  R. Sakakibara,et al.  Micturition-related neuronal firing in the periaqueductal gray area in cats , 2004, Neuroscience.

[38]  A. Shafik,et al.  Overactive bladder inhibition in response to pelvic floor muscle exercises , 2003, World Journal of Urology.

[39]  Ryuji Sakakibara,et al.  Micturitional disturbance after acute hemispheric stroke: analysis of the lesion site by CT and MRI , 1996, Journal of the Neurological Sciences.

[40]  Gert Holstege,et al.  Direct projections from the periaqueductal gray to the pontine micturition center (M-region). An anterograde and retrograde tracing study in the cat , 1994, Neuroscience Letters.

[41]  R. Sakakibara,et al.  Reduced cerebellar vermis activation during urinary storage and micturition in multiple system atrophy: 99mTc‐labelled ECD SPECT study , 2004, European journal of neurology.

[42]  S. Pomeroy,et al.  Neurological Dysfunction Associated With Postoperative Cerebellar Mutism , 2000, Journal of Neuro-Oncology.

[43]  B. Blok,et al.  Brain Control of the Lower Urinary Tract , 2002, Scandinavian journal of urology and nephrology. Supplementum.

[44]  C. Svarer,et al.  Cerebral activation during micturition in normal men. , 2000, Brain : a journal of neurology.