Brain, Vol. 123, No. 4, 781-789,
April 2000
© 2000 Oxford University Press
Cerebral activation during micturition in normal men
1 The Neurobiology Research Unit, N9201 and The PET and Cyclotron Unit, KF3982, The National University Hospital and 2 Department of Urology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
Correspondence to:
Ian Law, MD, The Neurobiology Research Unit, N 9201, Copenhagen University Hospital, Rigshospitalet, Blegdomsvej 9, DK-2100 Copenhagen, Denmark E-mail: ilaw{at}pet.rh.dk
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Specific cerebral lesions have shown the crucial role of the brain in the control of micturition. The precise identification of the anatomical cerebral structures involved in micturition can contribute to a better understanding of the control of micturition and the development of therapeutic models. Various neuropathological and animal studies have referred to the medulla oblongata, pons, limbic system, superior frontal lobe and premotor cortical regions as areas implicated in micturition control. The aim of this study was to investigate whether the activity of these areas during micturition can be confirmed by PET in normal men. The distribution of the regional cerebral blood flow after bolus injection of 15O water was used as an indirect measure of cerebral activation. PET scans were performed during the following three conditions: (i) at rest with the bladder empty; (ii) during simulated micturition after instillation of isotonic saline into the urinary bladder; and (iii) the withholding of urine (saline). Normal micturition using this model was achieved in eight out of 12 right-handed normal subjects. The changes in bladder contraction, bladder pressure and intra-abdominal pressure were monitored on-line during the whole scanning session by a cystometry device. The images were analysed using statistical parametric mapping at a significance threshold of P < 0.05 with correction for multiple independent comparisons. Micturition versus rest was associated with bilateral activation of areas close to the postcentral gyrus, inferior frontal gyrus, globus pallidus, cortex cerebelli, vermis and midbrain. On the left side, activation of the middle frontal gyrus, superior frontal gyrus, superior precentral gyrus, thalamus and the caudal part of the anterior cingulate gyrus was seen, while on the right side we found activation in the supramarginal gyrus, mesencephalon and insula. When the threshold value was lowered to P < 0.001 (Z > 3.09) without correction for multiple comparisons, we found additional activation in the medial pontine tegmentum, mesencephalon, right thalamus, right middle frontal gyrus and left insula. When urine- withholding was compared with rest, the left insula showed a tendency to activate. We conclude from this study, in which urinary bladder contraction was verified cystometrically, that the onset and maintenance of micturition in normal men is associated with a vast network of cortical and subcortical regions, confirming observations from clinical and animal studies.
PET; brain mapping; micturition; insula; frontal lobe
FD = first desire to void; ND = normal desire to void; PAG = periaqueductal grey matter; PMC = pontine micturition centre; SD = strong desire to void; SMA = supplementary motor area; SPECT = single photon emission computed tomography; SPM = statistical parametric mapping
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Introduction |
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Micturition is a complex process involving the coordination of functions that are under both voluntary and involuntary control. Thus, in spite of many clinical and animal studies and recent functional imaging studies there is still very little known about the central pathways and mechanisms behind the control of micturition.
Urinary incontinence is a common deficit associated with stroke (Kamouchi et al., 1995
; Sakakibara et al., 1996a, b), multiple sclerosis (Barbalias et al., 1998), Alzheimer's disease (Del-Ser et al., 1996), multiple system atrophy (Chandiramani et al., 1997), traumatic brain lesion (Kuru 1965), brain tumours (Yamagushi 1959), normal pressure hydrocephalus, Parkinson's disease (Jost et al., 1996) and other cerebral disorders.
Incontinence-provoking lesions can be located in the motor cortex (Kuru, 1965), the anterior and medial surfaces of the frontal lobe, the anterior edge of the paraventricular white matter, the genu of the internal capsule, the putamen, the thalamus (Sakakibara et al., 1996a) and the brainstem (Sakakibara et al., 1996b). Disorders located rostral to the pons almost always result in urge incontinence, while total disruption of the spinal cord always results in bladder–sphincter dyssynergia (an uncoordinated contraction of bladder and sphincter) (Schurch et al., 1994). Micturition must therefore be controlled by some region rostral to the pons and not by the spinal cord.
Earlier animal studies (Langworthy et al., 1936; Tang, 1955; Tang and Ruch, 1956; Mukai, 1959; Gjone et al., 1963; Yeates, 1974) have revealed that the motor cortex, the superomedial part of the frontal lobe, the anterior part of the cingulate gyrus and the genu of the corpus callosum have an inhibitory effect on two centres responsible for the initiation and coordination of micturition, viz. the hypothalamus and the pontine micturition centre (PMC). The physiology of micturition has been further elucidated by a more recent animal study (Fukuda et al., 1992) using somatosensory evoked potentials and electrocortical stimulation in dogs. This study suggests involvement of the sacral, hind leg and abdominal motor areas in the interruption of micturition through inhibition of the PMC and contraction of the external urethral sphincter.
Brain imaging studies of regional cerebral blood flow during behavioural activation offers a powerful tool for the non-invasive localization of sensorimotor and psychological functions. Two previous brain imaging studies of micturition (Fukuyama et al., 1996; Blok et al., 1997a) have confirmed the crucial role of frontal lobe and subcortical structures during micturition. A study by Fukuyama and colleagues using single photon emission computed tomography (SPECT) showed bilateral activation in the supplementary motor areas (SMA), the left sensorimotor area, the right frontal lobe, the pons and the midbrain during micturition (Fukuyama et al., 1996). Some of these results were confirmed by Blok and colleagues, who found significant activation in the right PMC, the periaqueductal grey (PAG), the hypothalamus and the right inferior frontal gyrus when comparing successful micturition with rest with the bladder empty (Blok et al., 1997a). These studies were performed without behavioural observation by cystometric recording and with the use of the subject's own urine production, which limited the number of scans performed per subject to one. Based on these considerations, we designed an experimental setup involving catheterization of subjects for cystometry, which allowed on-line recording of the pressure changes resulting from detrusor muscle activity during scanning. These recordings were used in further qualitative evaluation of the PET images. By infusion of isotonic saline, we were able to repeat conditions for each subject two to four times, producing a better foundation for the statistical analysis.
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Subjects
Twelve strongly right-handed (Oldfield, 1971
) healthy male volunteers were recruited (mean age 23.4 ± 1.1 years, range 22–25 years). No subject had a reported history of urological, psychiatric or neurological disease and all gave written informed consent according to the Helsinki II declaration, and the study was approved by the local ethics committee [J.nr. (KF) 01–406/96]. Two of the subjects were unable to void during scanning and an additional two subjects had delayed micturition; all four of these subjects were excluded from further analysis.
Activation paradigm
A few days before the scanning sessions the subjects were instructed to practise voiding in a horizontal position at home. None reported difficulty voiding in this position. Ten to twelve PET scans were completed under five conditions in a randomized order (at least two scans in each condition). All scans were performed with the eyes closed and covered, in a dim room. Only results from the comparisons of three of these conditions will be reported.
The three conditions were: (i) two scans at rest with the bladder empty; (ii) two to four scans during micturition after the bladder had been filled to the normal desire to void (ND); (iii) two scans during the withholding of urine (isotonic saline) after the bladder had been filled to ND.
The conditions not discussed in this paper are (i) interrupted micturition every third second cued by a metronome, and (ii) contractions of the urethral sphincter muscles at rest with the bladder empty every third second. These conditions will be published soon as a complementary part of the present study.
The subject's bladder was catheterized with two feeding tubes (100 cm, no. 5; Pharma-Plast International, Lynge, Denmark) and the bladder was emptied. The two intravesical catheters were connected to a cystometry device (Menuet; Dantec Medical, Skovlunde, Denmark) and used to fill the bladder with isotonic saline (temperature 37°C, infusion velocity 50 ml/min) and to monitor intravesical pressure, respectively. Voiding was possible without removing the catheters. A feeding tube (100 cm, no. 8; Pharma-Plast International) was placed in the rectum to monitor intra-abdominal pressure. After the initiation of isotonic saline infusion into the bladder, the subjects were asked to report the first sensation of bladder filling (FD, first desire to void) and, after further filling, to report ND. The water volumes infused at these points corresponded to the bladder volumes at FD and ND, respectively. The sensation at ND is normally stronger and of a longer duration than that at FD. A strong desire to void (SD) can be accomplished by further instillation of saline. Strong pain and sometimes the involuntary initiation of micturition characterize SD; therefore, ND was used in conditions (ii) and (iii). It should be noted that the FD, ND and SD are used in clinical cystometric evaluation of bladder capacity and are not constant between or within subjects; these definitions are therefore subjective and represent an attempt to standardize bladder stimulation to some degree.
During the whole scanning session, the cystometry device performed on-line analysis of detrusor pressure, measured by subtraction of the intra-abdominal from the intravesical pressure. The pressure was plotted against time (Fig. 1), and the increase in the detrusor pressure was used to confirm bladder contraction during scanning.
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Data acquisition
PET scanning
PET scans were obtained with an 18-ring GE-Advance scanner operating in 3D acquisition mode, producing 35 image slices with an interslice distance of 4.25 mm. The total axial field of view was 15.2 cm, with an in-plane resolution of ~5 mm. The technical specifications have been described elsewhere (DeGrado et al., 1994
). Every subject received 10–12 slow intravenous bolus injections of 400 MBq (11.4 mCi) of H215O with an interscan interval of 15 min. The isotope was administered through an antecubital intravenous catheter over 30 s (16 ml/min) by an automatic injection device. Head movement was limited by a head-holder constructed of thermally moulded foam. Before the activation session, a 10 min transmission scan was performed for attenuation correction. At the time of arrival of the bolus in the brain (~30 s after injection), the subjects were verbally instructed to void. The acquisition period was 90 s (Kanno et al., 1991). Images were reconstructed with a 4.0 mm Hanning filter transaxially and an 8.5 mm Ramp filter axially. The resulting distribution images of time-integrated counts were used as indirect measurements of the regional neural activity (Fox et al., 1989).
MRI scanning
Structural MRI scanning was performed with a 1.5 T Vision scanner (Siemens, Erlangen, Germany) using a 3D MPRAGE sequence (TR = 11 ms, TE = 4 ms, TI = 100 ms, flip angle = 15°). The images were acquired in the sagittal plane with an in-plane resolution of 0.98 mm and a slice thickness of 1.0 mm. The number of planes was 170 and the in-plane matrix dimensions were 256 x 256 voxels.
Image analysis
The complete brain volume was sampled for all subjects. Image analysis was performed using statistical parametric mapping software (SPM96; Wellcome Department of Cognitive Neurology, London, UK) (Frackowiak et al., 1994).
All intrasubject PET images were aligned using a 3D six-parameter rigid body transformation. The MRI image from each subject was co-registered to the corresponding average PET image and both image modalities were transformed into the standard stereotaxic atlas of Talairach and Tournoux (Talairach and Tournoux, 1988; Friston, 1994). The intersubject MRI average image was used for the anatomical localization of the activated areas. PET images were then smoothed with a 10 mm isotropic Gaussian filter to increase the signal-to-noise ratio and accommodate residual variability in morphological and topographical anatomy that was not accounted for by the stereotaxic normalization process (Friston et al., 1995). Differences in global activity were removed by proportional normalization of global brain counts to a value of 50.
The resulting set of voxel values constituted a statistical parametric map of the t statistic, SPM{t}. By transforming values from the SPM{t} into the unit Gaussian distribution using a probability integral transform, changes could be reported in Z scores (SPM{Z}). Voxels were considered significant if their Z score exceed a threshold of P < 0.05 with correction for multiple comparisons. The threshold value was subsequently dropped to P < 0.001 (Z > 3.09) without correction for multiple comparisons in order to detect activation tendencies. This threshold has also been used in a previous PET study reporting data on the activation pattern during micturition (Blok et al., 1997a). The resulting foci were then characterized in terms of the number of voxels (k) and peak Z score above this level.
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Cystometry
An increase in the average abdominal pressure during scanning was found in only three out of 21 successful cystometric recordings (range 2.3–7.4 cm H2O). The remaining measurements were all found to be close to the noise level (range 2.1–1.8 cm H2O).
The detrusor pressure curves (Fig. 1
) were analysed to determine mean and maximum detrusor pressure and detrusor contraction time for each subject under the different conditions (Table 1). The mean and maximum detrusor pressures and the detrusor contraction times were used to document bladder contraction throughout the scanning period. Using paired t tests, we found no significant differences at a threshold level of P < 0.05 between urine withholding and micturition mean bladder volume at ND. Due to errors in data storage, not all cystometric recordings could be analysed post hoc. The numbers of successful recordings compared with the total numbers of micturition PET scans can be seen in Table 1. It should be noted, however, that the pressure changes were monitored on-line and that detrusor pressure changes were observed throughout all micturition scans. The ND volume was recorded before each scan, and thus no data were lost.
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PET results
Urine withholding versus rest
When the urine-withholding condition was compared with rest, no areas showed significant activation (with correction for multiple comparison), but there was a tendency to activation (without correction for multiple comparison) in the left insula (x = –40, y = 14, z = 2).
Micturition versus rest
Areas with significant activation.
The micturition condition compared with rest was associated with bilateral activation of areas close to the postcentral gyrus, inferior frontal gyrus, globus pallidus, midbrain, vermis and cortex cerebelli. On the left side, additional activation of the superior precentral gyrus, middle frontal gyrus, superior frontal gyrus, thalamus and caudal part of anterior cingulate gyrus was seen, whereas on the right side we found additional activation in the supramarginal gyrus, the central part of the mesencephalon on the right side of aqueductus cerebri and insula (Table 2 and Fig. 2).
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Activation tendencies.
When the threshold value was dropped to P < 0.001 (Z > 3.09) without correction for multiple comparisons, we found additional activation in the medial pontine tegmentum, mesencephalon, right thalamus, right middle frontal gyrus and left insula.
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The cortical structures
It should be noted that micturition is a complex process involving both voluntary and involuntary control and that the active micturition scans in this study involved both the onset and the maintenance of micturition. The activation in the left pre- and postcentral gyri during micturition probably corresponds to activation of the abdominal sensorimotor region while the activation in the left middle frontal gyrus represents the SMA. A similar pattern has been demonstrated in a SPECT micturition study by Fukuyama and colleagues, who found activation in the left sensorimotor cortex and right lateral frontal cortex and bilateral activation in the SMA when comparing micturition with rest (Fukuyama et al., 1996
). Our study is the first to employ cystometric recording in the behavioural characterization of micturition during scanning. Although the catheters are also in place during the resting condition when this technique is used, it is possible that they can lead to micturition-related sensory stimulation. In part, this could be due to increased resistance to urine outflow, which could increase the stimulation of bladder stretch receptors. As these receptors would also be stimulated during normal micturition, it is reasonable to assume that the cerebral areas involved in the sensory perception are unchanged, although the regional activity might be increased. That the activation in this sensorimotor area is not solely an artefact of catheterization is supported by a study performed during normal micturition in which a similar activation was found (Fukuyama et al., 1996). Although the change in abdominal pressure in the present study was modest, the relationship between intra-abdominal pressure and cerebral activation has not been studied in detail. Our activated foci are located close to areas found during the contraction of the pelvic floor and abdominal muscles (Blok et al., 1997b), and therefore we cannot exclude this component.
The abdominal sensory motor cortex was not sampled in the study by Blok and colleagues (Blok et al., 1997a), in which the actual field of view of the PET scanner used was limited; this restricted sampling to areas below 44 mm in Talairach space.
Sakakibara and colleagues have shown that lesions particularly in the frontal lobe or its descending pathways at the anterior edge of the paraventricular white matter, the genu of the internal capsule, the putamen or the thalamus result in micturitional disturbance (Sakakibara et al., 1996a). This suggests that it is mainly lesions in the anteromedial frontal lobe and its descending pathways and the basal ganglia that are responsible for detrusor hyper-reflexia. Additionally, a study of 36 patients suffering from cerebrovascular accidents causing hemiplegia and continence disorders performed by Thiry and colleagues has pointed to the motor cortex as one region that is crucial in the inability to interrupt micturition in patients with continence disorders (Thiry et al., 1989). These authors report that, when the bladder was empty, transcranial stimulation of the vertex resulted in contraction of the external urethral sphincter, whereas during micturition this stimulation had no micturition-interrupting effect. They concluded that, in these patients, either the central motor pathway was inhibited by other central circuits or the central motor volley itself failed to depolarize the inhibited sphincter lower motor neurons above their firing threshold.
During micturition we found bilateral activation in the inferior frontal gyrus as well as a tendency towards activation in the left superior frontal gyrus. Likewise, Fukuyama and colleagues and Blok and colleagues reported activation in the right lateral frontal cortex and the right inferior frontal gyrus when comparing similar conditions (Fukuyama et al., 1996; Blok et al., 1997a). The prefrontal lobes possibly play an important role in deciding whether to initiate micturition by direct connections to subcortical regions.
Apart from the motor cortex, the premotor cortex and the medial frontal gyrus, the comparison of micturition and rest demonstrated activation in other areas related to voluntary motor control, such as the anterior cingulate gyrus and the cerebellum. This pattern of activation could reflect the involvement of voluntary motor control over the autonomic nervous system in micturition. In many ways this resembles findings during volitional breathing (Colebatch et al., 1991).
Urodynamic evaluation of patients with cerebellar ataxia (Prati et al., 1993) and investigations in animals involving cerebellectomy (Nishizawa et al., 1989) suggest an inhibitory role of the cerebellum in the storage phase and a possible facilitatory role in the emptying phase of micturition. Blok and colleagues also found the cerebellum to be activated significantly during straining of the pelvic muscles in women (Blok et al., 1997b). It is possible that the cerebellum regulates detrusor muscle tone during both urine storage and the micturition phase. We also found that the vermis was activated during micturition. Intricate connections exist between the hypothalamus and the anterior cerebellar vermis which could supply the anatomical substrate for the regulation of autonomic responses such as micturition (Supple, 1993).
Subcortical structures
In comparing micturition versus rest, this study showed bilateral activation in the globus pallidus and the cortex cerebelli as well as activation in the anterior and posterior parts of the midbrain and in vermis, left thalamus and right insula (Fig. 2 and Table 2). Activation in the midbrain possibly represents activation in the rostral part of the hypothalamus and the tegmental part of the PAG (Fig. 2E and H). A region in the pons (possibly PMC) and tegmentum (possibly PAG) also showed a tendency to activate (Table 2). Fukuyama and colleagues have reported activation in the midbrain and pons when comparing micturition versus rest (Fukuyama et al., 1996). Additionally, Blok and colleagues have demonstrated activation in the hypothalamus, areas close to the PAG, the right dorsomedial pons, the right dorsomedial pontine tegmentum and the rostral hypothalamus when comparing successful micturition with rest with the bladder empty (Blok et al., 1997a). None of these authors have reported any activation in the thalamus, insula or globus pallidus; some of these activated areas may therefore reflect stimulation of the bladder and urethra by the catheter. On the other hand, activity of these structures could be due to the involvement of a complex network of cortical and subcortical structures during the onset and maintenance of micturition.
The most recent model of the control of micturition is based on studies performed by Blok and Holstege (Blok and Holstege, 1994) and Blok and colleagues (Blok et al., 1995, 1997a). According to this model, information about the degree of bladder-filling is sent from neurons in the lumbosacral cord to the PAG, an area known for its involvement in nociception (Mantyh 1982), micturition and many other vital functions. When the bladder is filled near to its capacity and voiding is appropriate, the PAG activates an area in the dorsomedial pontine tegmentum referred to as the M region or PMC. The PMC in turn initiates a complete synergic micturition response through the descending parasympathetic bladder motor neurons in the sacral part of the spinal cord. It has been suggested that PAG activation results from bladder stretch receptor activity, which in turn activates the PMC (Vanderhorst et al., 1996). On the other hand, when comparing the withholding of urine with rest with the bladder empty, neither the present study nor previous studies have reported significant activation in the PAG. So either the activation of the PAG in this state is not detectable by PET or the distension of the bladder near to its capacity alone is not what gives rise to PAG activation. Activation of the PAG during micturition may be responsible for disinhibition of the PMC. The remaining question is how the PAG is controlled. It has been shown that the rostral part of the hypothalamus not only has descending pathways to the PAG (Holstege, 1995) but is also the only region in the midbrain that projects directly to the PMC (Holstege, 1987). Micturition may be initiated through activation of the hypothalamus, which in turn activates the PAG, resulting in disinhibition of the PMC, which in turn coordinates micturition. Inhibition of the PMC, on the other hand, may occur via the descending projections of the abdominal sensorimotor area, also resulting in contraction of the external urethral sphincter (Fukuda et al., 1992). A recent MRI study of patients with urinary disorders after an acute brainstem stroke (Sakakibara et al., 1996b) verifies the pons as a region that is crucial in the control of micturition. This study showed correlation between urinary disorders and lesions concentrated in the dorsolateral pons, including the pontine reticular nucleus and the reticular formation adjacent to the medial parabrachial nucleus and the locus coeruleus.
Subtracting urine-withholding scans at ND from rest with the bladder empty, we found a tendency towards activation only in the left anterior insula. Hsieh and colleagues demonstrated that chronic ongoing neuropathic pain in man results in activation of the anterior insula but not activation of the somatosensory areas (Hsieh et al., 1995). It has also been suggested (Saper, 1982) that insular cortex may represent a cortical region for the integration of the limbic and the autonomic response. The activation of the insula during the withholding of urine could be due to visceral sensory feedback from the stretch receptor activity of the bladder, the autonomic regulation of the micturition process or the stimulation of the bladder and urethra by catheters.
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Acknowledgments |
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We wish to thank Rikke Permild, Karin Stahr and the staff of the PET centre at the Rigshospitalet, Copenhagen. This work was supported by a grant from the Danish Medical Research Council and the Danish Foundation for the Advancement of Medical Science. The John and Birthe Meyer Foundation is gratefully acknowledged for the donation of the Cyclotron and PET scanner.
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Received August 2, 1999. Revised October 4, 1999. Accepted October 20, 1999.
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