Abstract
Neural circuitry regulating urine storage in humans has been largely inferred from fMRI during urodynamic studies driven by catheter infusion of fluid into the bladder. However, urodynamic testing may be confounded by artificially filling the bladder repeatedly at a high rate and examining associated time-locked changes in fMRI signals. Here we describe and test a more ecologically-valid paradigm to study the brain response to bladder filling by (1) filling the bladder naturally with oral water ingestion, (2) examining resting state fMRI (rs-fMRI) which is more natural since it is not linked with a specific stimulus, and (3) relating rs-fMRI measures to self-report (urinary urge) and physiologic measures (voided volume). To establish appropriate controls and analyses for future clinical studies, here we analyze data collected from healthy individuals (N = 62) as part of the Multidisciplinary Approach to the Study of Chronic Pelvic Pain (MAPP) Research Network. Participants orally ingested approximately 350 mL of water, and had a 10 min “fuller bladder” rs-fMRI scan approximately 1 h later. A second 10 min “empty bladder” rs-fMRI scan was conducted immediately following micturition. We examined multiple spatial scales of brain function, including local activity, circuits, and networks. We found changes in brain function distributed across micturition loci (e.g., subregions of the salience, sensorimotor, and default networks) that were significantly related to the stimulus (volume) and response (urinary urge). Based on our results, this paradigm can be applied in the future to study the neurobiological underpinnings of urologic conditions.
Highlights
The central nervous system (CNS) communicates with the bladder to signal when micturition should occur[1,2,3]
We address the proportion of participants in whom the paradigm induced urinary urge, the association between self-report and physiologic measures, and examine three resting state functional Magnetic Resonance Imaging (fMRI) (rs-fMRI) analysis techniques, each operating at a different spatial scale, to quantify brain response to natural bladder filling
We found a significant correlation between the difference in urinary urge between the rs-fuller” bladder (FB) and rs-empty bladder (EB) scans and the volume voided after the rs-FB scan, which we interpret as a surrogate for the volume of fluid in the bladder during the rs-FB scan (Fig. 2B)
Summary
The central nervous system (CNS) communicates with the bladder to signal when micturition should occur[1,2,3]. Over the past two decades, noninvasive functional brain imaging has shed light on the multiple brain regions involved in regulating the b ladder[1,8] These encompass midbrain and subcortical structures [pontine micturition center, periaqueductal gray (PAG), thalamus] and cortical structures (supplementary motor area, insular cortex, anterior cingulate, prefrontal cortex), which have been reviewed p reviously[8]. Urodynamic testing in fMRI has an advantage of improved experimental control over bladder volume, it has several limitations This procedure fills the bladder at supraphysiologic rates through an artificial mechanism; the brain response reported in these studies may be partially driven by salience, attention, patient discomfort and anxiety, and other factors that are beyond actual bladder activity. The MAPP-II bladder filling paradigm needed to (1) be tolerable to patients with UCPPS, (2) evoke an urge to urinate and a brain response in healthy individuals to provide suitable controls, and (3) had to provide assessments of pain, urinary urge, and voided volume at critical time points
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