Exercise modulates neuronal activation in the micturition circuit of chronically stressed rats: A multidisciplinary approach to the study of urologic chronic pelvic pain syndrome (MAPP) research network study
•We examine effects of exercise on urinary voiding and brain function in rats.•Wheel running reverses stress-associated patterns in urinary voiding.•Exercise elicits differential effects on brain activation during bladder distension.•Alteration is noted in the reflex micturition and corticolimbic co...
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| creator | Holschneider, Daniel P. Wang, Zhuo Guo, Yumei Sanford, Melissa T. Yeh, Jihchao Mao, Jackie J. Zhang, Rong Rodriguez, Larissa V. |
| description | •We examine effects of exercise on urinary voiding and brain function in rats.•Wheel running reverses stress-associated patterns in urinary voiding.•Exercise elicits differential effects on brain activation during bladder distension.•Alteration is noted in the reflex micturition and corticolimbic control circuits.•Exercise is proposed as an adjunct therapy for urinary frequency and urgency.
Rats exposed to water avoidance stress (WAS) show increased urinary frequency, increased somatosensory nociceptive reflex responses, as well as altered brain responses to bladder distension, analogous to similar observations made in patients with urologic chronic pelvic pain syndrome (UCPPS). Exercise has been proposed as a potential treatment option for patients with chronic urinary frequency and urgency. We examined the effects of exercise on urinary voiding parameters and functional brain activation during bladder distension in rats exposed to WAS.
Adult, female Wistar Kyoto rats were exposed to 10 days of WAS and thereafter randomized to either voluntary exercise for 3 weeks or sedentary groups. Voiding parameters were assessed at baseline, post-WAS, and weekly for 3 weeks. Thereafter, cerebral blood flow (CBF) mapping was performed during isotonic bladder distension (20 cm H2O) after intravenous bolus injection of [14C]-iodoantipyrine. Regional CBF was quantified in autoradiographs of brain slices and analyzed in 3-D reconstructed brains by statistical parametric mapping. Functional connectivity was examined between regions of the micturition circuit through interregional correlation analysis.
WAS exposure in sedentary animals (WAS/no-EX) increased voiding frequency and decreased urinary volumes per void. Exercise exposure in WAS animals (WAS/EX) resulted in a progressive decline in voiding frequency back to the baseline, as well as increased urinary volumes per void. Within the micturition circuit, WAS/EX compared to WAS/no-EX demonstrated a significantly lower rCBF response to passive bladder distension in Barrington's nucleus that is part of the spinobulbospinal voiding reflex, as well as in the periaqueductal gray (PAG) which modulates this reflex. Greater rCBF was noted in WAS/EX animals broadly across corticolimbic structures, including the cingulate, medial prefrontal cortex (prelimbic, infralimbic areas), insula, amygdala, and hypothalamus, which provide a ‘top-down’ decision point where micturition could be inhibited or triggered. WAS/EX showed a significa |
| doi_str_mv | 10.1016/j.physbeh.2019.112796 |
| format | Article |
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Rats exposed to water avoidance stress (WAS) show increased urinary frequency, increased somatosensory nociceptive reflex responses, as well as altered brain responses to bladder distension, analogous to similar observations made in patients with urologic chronic pelvic pain syndrome (UCPPS). Exercise has been proposed as a potential treatment option for patients with chronic urinary frequency and urgency. We examined the effects of exercise on urinary voiding parameters and functional brain activation during bladder distension in rats exposed to WAS.
Adult, female Wistar Kyoto rats were exposed to 10 days of WAS and thereafter randomized to either voluntary exercise for 3 weeks or sedentary groups. Voiding parameters were assessed at baseline, post-WAS, and weekly for 3 weeks. Thereafter, cerebral blood flow (CBF) mapping was performed during isotonic bladder distension (20 cm H2O) after intravenous bolus injection of [14C]-iodoantipyrine. Regional CBF was quantified in autoradiographs of brain slices and analyzed in 3-D reconstructed brains by statistical parametric mapping. Functional connectivity was examined between regions of the micturition circuit through interregional correlation analysis.
WAS exposure in sedentary animals (WAS/no-EX) increased voiding frequency and decreased urinary volumes per void. Exercise exposure in WAS animals (WAS/EX) resulted in a progressive decline in voiding frequency back to the baseline, as well as increased urinary volumes per void. Within the micturition circuit, WAS/EX compared to WAS/no-EX demonstrated a significantly lower rCBF response to passive bladder distension in Barrington's nucleus that is part of the spinobulbospinal voiding reflex, as well as in the periaqueductal gray (PAG) which modulates this reflex. Greater rCBF was noted in WAS/EX animals broadly across corticolimbic structures, including the cingulate, medial prefrontal cortex (prelimbic, infralimbic areas), insula, amygdala, and hypothalamus, which provide a ‘top-down’ decision point where micturition could be inhibited or triggered. WAS/EX showed a significantly greater positive brain functional connectivities compared to WAS/no-EX animals within regions of the extended reflex loop (PAG, Barrington's nucleus, intermediodorsal thalamic nucleus, pons), as well as within regions of the corticolimbic decision-making loop of the micturition circuit, with a strikingly negative correlation between these pathways. Urinary frequency was positively correlated with rCBF in the pons, and negatively correlated with rCBF in the cingulate cortex.
Our results suggest that chronic voluntary exercise may decrease urinary frequency at two points of control in the micturition circuit. During the urine storage phase, it may diminish the influence of the reflex micturition circuit itself, and/or it may increase corticolimbic control of voiding. Exercise may be an effective adjunct therapeutic intervention for modifying the urinary symptoms in patients with UCPPS.</description><identifier>ISSN: 0031-9384</identifier><identifier>ISSN: 1873-507X</identifier><identifier>EISSN: 1873-507X</identifier><identifier>DOI: 10.1016/j.physbeh.2019.112796</identifier><identifier>PMID: 31884113</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Autoradiography ; Bladder pain syndrome ; Brain Mapping ; Cerebral Cortex - physiopathology ; Cerebrovascular Circulation ; Exercise ; Female ; Functional brain mapping ; Interstitial cystitis ; Limbic System - physiopathology ; Micturition circuit ; Neural Pathways - physiopathology ; Pelvic Pain - physiopathology ; Physical Conditioning, Animal - physiology ; Psychological stress ; Rats ; Rats, Inbred WKY ; Sedentary Behavior ; Stress, Psychological - physiopathology ; Urinary Bladder - physiopathology ; Urination - physiology</subject><ispartof>Physiology & behavior, 2020-03, Vol.215, p.112796-112796, Article 112796</ispartof><rights>2019 Elsevier Inc.</rights><rights>Copyright © 2019 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c533t-cf3fb2d1e3c53562855d6666cf8bac141b7692ca8f2ad01f9253db6b8bb5ba5d3</citedby><cites>FETCH-LOGICAL-c533t-cf3fb2d1e3c53562855d6666cf8bac141b7692ca8f2ad01f9253db6b8bb5ba5d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0031938419308698$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3536,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31884113$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Holschneider, Daniel P.</creatorcontrib><creatorcontrib>Wang, Zhuo</creatorcontrib><creatorcontrib>Guo, Yumei</creatorcontrib><creatorcontrib>Sanford, Melissa T.</creatorcontrib><creatorcontrib>Yeh, Jihchao</creatorcontrib><creatorcontrib>Mao, Jackie J.</creatorcontrib><creatorcontrib>Zhang, Rong</creatorcontrib><creatorcontrib>Rodriguez, Larissa V.</creatorcontrib><title>Exercise modulates neuronal activation in the micturition circuit of chronically stressed rats: A multidisciplinary approach to the study of urologic chronic pelvic pain syndrome (MAPP) research network study</title><title>Physiology & behavior</title><addtitle>Physiol Behav</addtitle><description>•We examine effects of exercise on urinary voiding and brain function in rats.•Wheel running reverses stress-associated patterns in urinary voiding.•Exercise elicits differential effects on brain activation during bladder distension.•Alteration is noted in the reflex micturition and corticolimbic control circuits.•Exercise is proposed as an adjunct therapy for urinary frequency and urgency.
Rats exposed to water avoidance stress (WAS) show increased urinary frequency, increased somatosensory nociceptive reflex responses, as well as altered brain responses to bladder distension, analogous to similar observations made in patients with urologic chronic pelvic pain syndrome (UCPPS). Exercise has been proposed as a potential treatment option for patients with chronic urinary frequency and urgency. We examined the effects of exercise on urinary voiding parameters and functional brain activation during bladder distension in rats exposed to WAS.
Adult, female Wistar Kyoto rats were exposed to 10 days of WAS and thereafter randomized to either voluntary exercise for 3 weeks or sedentary groups. Voiding parameters were assessed at baseline, post-WAS, and weekly for 3 weeks. Thereafter, cerebral blood flow (CBF) mapping was performed during isotonic bladder distension (20 cm H2O) after intravenous bolus injection of [14C]-iodoantipyrine. Regional CBF was quantified in autoradiographs of brain slices and analyzed in 3-D reconstructed brains by statistical parametric mapping. Functional connectivity was examined between regions of the micturition circuit through interregional correlation analysis.
WAS exposure in sedentary animals (WAS/no-EX) increased voiding frequency and decreased urinary volumes per void. Exercise exposure in WAS animals (WAS/EX) resulted in a progressive decline in voiding frequency back to the baseline, as well as increased urinary volumes per void. Within the micturition circuit, WAS/EX compared to WAS/no-EX demonstrated a significantly lower rCBF response to passive bladder distension in Barrington's nucleus that is part of the spinobulbospinal voiding reflex, as well as in the periaqueductal gray (PAG) which modulates this reflex. Greater rCBF was noted in WAS/EX animals broadly across corticolimbic structures, including the cingulate, medial prefrontal cortex (prelimbic, infralimbic areas), insula, amygdala, and hypothalamus, which provide a ‘top-down’ decision point where micturition could be inhibited or triggered. WAS/EX showed a significantly greater positive brain functional connectivities compared to WAS/no-EX animals within regions of the extended reflex loop (PAG, Barrington's nucleus, intermediodorsal thalamic nucleus, pons), as well as within regions of the corticolimbic decision-making loop of the micturition circuit, with a strikingly negative correlation between these pathways. Urinary frequency was positively correlated with rCBF in the pons, and negatively correlated with rCBF in the cingulate cortex.
Our results suggest that chronic voluntary exercise may decrease urinary frequency at two points of control in the micturition circuit. During the urine storage phase, it may diminish the influence of the reflex micturition circuit itself, and/or it may increase corticolimbic control of voiding. Exercise may be an effective adjunct therapeutic intervention for modifying the urinary symptoms in patients with UCPPS.</description><subject>Animals</subject><subject>Autoradiography</subject><subject>Bladder pain syndrome</subject><subject>Brain Mapping</subject><subject>Cerebral Cortex - physiopathology</subject><subject>Cerebrovascular Circulation</subject><subject>Exercise</subject><subject>Female</subject><subject>Functional brain mapping</subject><subject>Interstitial cystitis</subject><subject>Limbic System - physiopathology</subject><subject>Micturition circuit</subject><subject>Neural Pathways - physiopathology</subject><subject>Pelvic Pain - physiopathology</subject><subject>Physical Conditioning, Animal - physiology</subject><subject>Psychological stress</subject><subject>Rats</subject><subject>Rats, Inbred WKY</subject><subject>Sedentary Behavior</subject><subject>Stress, Psychological - physiopathology</subject><subject>Urinary Bladder - physiopathology</subject><subject>Urination - physiology</subject><issn>0031-9384</issn><issn>1873-507X</issn><issn>1873-507X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFksFu1DAQhi0EokvhEUA-lkOW2E6yCQfQqmoBqYgeQOJmOfak8eLYwXYW8pZ9JLzNtoITcxnZ_uf7bc8g9JLka5KT6s1uPfZzaKFf05w0a0LopqkeoRWpNywr8833x2iV54xkDauLE_QshF2eghXsKTphpK4LQtgK3V78Bi91ADw4NRkRIWALk3dWGCxk1HsRtbNYWxz7JNIyTl7fbUnt5aQjdh2WfSrQUhgz4xA9hAAKexHDW7zFw2SiVjpIPRpthZ-xGEfvhOxxdHfUECc1HzjJ17gbLe-BeASzPySR_MNslXcD4LPP2-vr1zjZgPCJYiH-cv7HgnmOnnTCBHhxzKfo2-XF1_OP2dWXD5_Ot1eZLBmLmexY11JFgKV1WdG6LFWVQnZ1KyQpSLupGipF3VGhctI1tGSqrdq6bctWlIqdoncLd5zaAZQEG70wfPR6SE_kTmj-74nVPb9xe76hVVPlLAHOjgDvfk4QIh_SH4ExwoKbAqeMkYI2tCiStFyk0rsQPHQPNiTnh2ngO36cBn6YBr5MQ6p79fcdH6ru258E7xcBpJ_aa_A8dQmsBKU9yMiV0_-x-ANUhNF-</recordid><startdate>20200301</startdate><enddate>20200301</enddate><creator>Holschneider, Daniel P.</creator><creator>Wang, Zhuo</creator><creator>Guo, Yumei</creator><creator>Sanford, Melissa T.</creator><creator>Yeh, Jihchao</creator><creator>Mao, Jackie J.</creator><creator>Zhang, Rong</creator><creator>Rodriguez, Larissa V.</creator><general>Elsevier Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20200301</creationdate><title>Exercise modulates neuronal activation in the micturition circuit of chronically stressed rats: A multidisciplinary approach to the study of urologic chronic pelvic pain syndrome (MAPP) research network study</title><author>Holschneider, Daniel P. ; Wang, Zhuo ; Guo, Yumei ; Sanford, Melissa T. ; Yeh, Jihchao ; Mao, Jackie J. ; Zhang, Rong ; Rodriguez, Larissa V.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c533t-cf3fb2d1e3c53562855d6666cf8bac141b7692ca8f2ad01f9253db6b8bb5ba5d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Autoradiography</topic><topic>Bladder pain syndrome</topic><topic>Brain Mapping</topic><topic>Cerebral Cortex - physiopathology</topic><topic>Cerebrovascular Circulation</topic><topic>Exercise</topic><topic>Female</topic><topic>Functional brain mapping</topic><topic>Interstitial cystitis</topic><topic>Limbic System - physiopathology</topic><topic>Micturition circuit</topic><topic>Neural Pathways - physiopathology</topic><topic>Pelvic Pain - physiopathology</topic><topic>Physical Conditioning, Animal - physiology</topic><topic>Psychological stress</topic><topic>Rats</topic><topic>Rats, Inbred WKY</topic><topic>Sedentary Behavior</topic><topic>Stress, Psychological - physiopathology</topic><topic>Urinary Bladder - physiopathology</topic><topic>Urination - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Holschneider, Daniel P.</creatorcontrib><creatorcontrib>Wang, Zhuo</creatorcontrib><creatorcontrib>Guo, Yumei</creatorcontrib><creatorcontrib>Sanford, Melissa T.</creatorcontrib><creatorcontrib>Yeh, Jihchao</creatorcontrib><creatorcontrib>Mao, Jackie J.</creatorcontrib><creatorcontrib>Zhang, Rong</creatorcontrib><creatorcontrib>Rodriguez, Larissa V.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Physiology & behavior</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Holschneider, Daniel P.</au><au>Wang, Zhuo</au><au>Guo, Yumei</au><au>Sanford, Melissa T.</au><au>Yeh, Jihchao</au><au>Mao, Jackie J.</au><au>Zhang, Rong</au><au>Rodriguez, Larissa V.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Exercise modulates neuronal activation in the micturition circuit of chronically stressed rats: A multidisciplinary approach to the study of urologic chronic pelvic pain syndrome (MAPP) research network study</atitle><jtitle>Physiology & behavior</jtitle><addtitle>Physiol Behav</addtitle><date>2020-03-01</date><risdate>2020</risdate><volume>215</volume><spage>112796</spage><epage>112796</epage><pages>112796-112796</pages><artnum>112796</artnum><issn>0031-9384</issn><issn>1873-507X</issn><eissn>1873-507X</eissn><abstract>•We examine effects of exercise on urinary voiding and brain function in rats.•Wheel running reverses stress-associated patterns in urinary voiding.•Exercise elicits differential effects on brain activation during bladder distension.•Alteration is noted in the reflex micturition and corticolimbic control circuits.•Exercise is proposed as an adjunct therapy for urinary frequency and urgency.
Rats exposed to water avoidance stress (WAS) show increased urinary frequency, increased somatosensory nociceptive reflex responses, as well as altered brain responses to bladder distension, analogous to similar observations made in patients with urologic chronic pelvic pain syndrome (UCPPS). Exercise has been proposed as a potential treatment option for patients with chronic urinary frequency and urgency. We examined the effects of exercise on urinary voiding parameters and functional brain activation during bladder distension in rats exposed to WAS.
Adult, female Wistar Kyoto rats were exposed to 10 days of WAS and thereafter randomized to either voluntary exercise for 3 weeks or sedentary groups. Voiding parameters were assessed at baseline, post-WAS, and weekly for 3 weeks. Thereafter, cerebral blood flow (CBF) mapping was performed during isotonic bladder distension (20 cm H2O) after intravenous bolus injection of [14C]-iodoantipyrine. Regional CBF was quantified in autoradiographs of brain slices and analyzed in 3-D reconstructed brains by statistical parametric mapping. Functional connectivity was examined between regions of the micturition circuit through interregional correlation analysis.
WAS exposure in sedentary animals (WAS/no-EX) increased voiding frequency and decreased urinary volumes per void. Exercise exposure in WAS animals (WAS/EX) resulted in a progressive decline in voiding frequency back to the baseline, as well as increased urinary volumes per void. Within the micturition circuit, WAS/EX compared to WAS/no-EX demonstrated a significantly lower rCBF response to passive bladder distension in Barrington's nucleus that is part of the spinobulbospinal voiding reflex, as well as in the periaqueductal gray (PAG) which modulates this reflex. Greater rCBF was noted in WAS/EX animals broadly across corticolimbic structures, including the cingulate, medial prefrontal cortex (prelimbic, infralimbic areas), insula, amygdala, and hypothalamus, which provide a ‘top-down’ decision point where micturition could be inhibited or triggered. WAS/EX showed a significantly greater positive brain functional connectivities compared to WAS/no-EX animals within regions of the extended reflex loop (PAG, Barrington's nucleus, intermediodorsal thalamic nucleus, pons), as well as within regions of the corticolimbic decision-making loop of the micturition circuit, with a strikingly negative correlation between these pathways. Urinary frequency was positively correlated with rCBF in the pons, and negatively correlated with rCBF in the cingulate cortex.
Our results suggest that chronic voluntary exercise may decrease urinary frequency at two points of control in the micturition circuit. During the urine storage phase, it may diminish the influence of the reflex micturition circuit itself, and/or it may increase corticolimbic control of voiding. Exercise may be an effective adjunct therapeutic intervention for modifying the urinary symptoms in patients with UCPPS.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>31884113</pmid><doi>10.1016/j.physbeh.2019.112796</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Autoradiography Bladder pain syndrome Brain Mapping Cerebral Cortex - physiopathology Cerebrovascular Circulation Exercise Female Functional brain mapping Interstitial cystitis Limbic System - physiopathology Micturition circuit Neural Pathways - physiopathology Pelvic Pain - physiopathology Physical Conditioning, Animal - physiology Psychological stress Rats Rats, Inbred WKY Sedentary Behavior Stress, Psychological - physiopathology Urinary Bladder - physiopathology Urination - physiology |
| title | Exercise modulates neuronal activation in the micturition circuit of chronically stressed rats: A multidisciplinary approach to the study of urologic chronic pelvic pain syndrome (MAPP) research network study |
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