Plasma Protein Extravasation Induced in the Rat Dura Mater by Stimulation of the Parasympathetic Sphenopalatine Ganglion

Delepine, Laurent; Aubineau, P.

doi:10.1006/exnr.1997.6614

Cited by 66 publications

(52 citation statements)

References 37 publications

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“…Second, preganglionic fibers in the hypogastric nerve synapse not only on neurons in the inferior mesenteric ganglion but also on neurons in the pelvic ganglion (23, 68), i.e., the pelvic ganglion receives preganglionic input from fibers traveling in both the hypogastric nerve derived from T13/L1 and the pelvic nerve derived from L6-S2. Third, whereas centrally generated activation of postganglionic sympathetic fibers fails to elicit PE (48), activation of postganglionic parasympathetic efferents does elicit extravasation (3,20). Thus it is possible that input from the inflamed organ via the hypogastric nerve activates neurons in the dorsal horn of T13/L1 that in turn eventually activate postganglionic neurons in the pelvic ganglion via three different multisynaptic routes: 1) preganglionic neurons in T13/L1 (Fig.…”

Section: Discussionmentioning

confidence: 99%

Cross-organ interactions between reproductive, gastrointestinal, and urinary tracts: modulation by estrous stage and involvement of the hypogastric nerve

Winnard¹,

Dmitrieva²,

Berkley³

2006

American Journal of Physiology-Regulatory, Integrative and Comp

101

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-Central nervous system neurons process information converging from the uterus, colon, and bladder, partly via the hypogastric nerve. This processing is influenced by the estrous cycle, suggesting the existence of an estrous-modifiable central nervous system substrate by which input from one pelvic organ can influence functioning of other pelvic organs. Here, we tested predictions from this hypothesis that acute inflammation of colon, uterine horn, or bladder would produce signs of inflammation in the other uninflamed organs (increase vascular permeability) and that cross-organ effects would vary with estrous and be eliminated by hypogastric neurectomy (HYPX). Under urethane anesthesia, the colon, uterine horn, or bladder of rats in proestrus or metestrus, with or without prior HYPX, was treated with mustard oil or saline. Two hours later, Evans Blue dye extravasation was measured to assess vascular permeability. Extravasation was increased in all inflamed organs, regardless of estrous stage. For rats in proestrus, but not metestrus, either colon or uterine horn inflammation significantly increased extravasation in the uninflamed bladder. Much smaller cross-organ effects were seen in colon and uterine horn. HYPX reduced extravasation in the inflamed colon and inflamed uterine horn, but not the inflamed bladder. HYPX eliminated the colon-to-bladder and uterine horn-to-bladder effects. These results demonstrate that inflaming one pelvic organ can produce estrous-modifiable signs of inflammation in other pelvic organs, particularly bladder, and suggest that the cross-organ effects involve the hypogastric nerve and are at least partly centrally mediated. Such effects could contribute to cooccurrence and cyclicity of distressing pelvic disorders in women. pelvic pain; inflammation; interstitial cystitis; uterus; colon NEURAL COORDINATION AND decision-making for many physiological and behavioral functions depends on convergence within the nervous system of information from different bodily regions (for example, see Ref 4). Such is the case, for example, in the control of walking, balance, posture, eye movements, blood pressure, fight/flight responses, and other sensorimotor functions (39). Much of this convergence involves heterotopic interactions between different somatic structures (muscles/ skin) or between somatic and visceral structures.Such coordination is less well understood between different internal organs; that is, viscerovisceral interactions. Studies have shown, however, that neurons in the spinal cord, dorsal column nuclei, solitary nucleus, medullary reticular formation, and thalamus process information that converges from different internal organs located in different functional systems, i.e., the reproductive, gastrointestinal, and urinary tracts (8,9,11,17,24,31,32,37,57,58,59,60). In some regions, this processing is robustly influenced by the estrous cycle and hormone manipulations (15,16).This cross-system, viscerovisceral convergence supports the concept that the nervous system provides a dynamic ...

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Section: Discussionmentioning

confidence: 99%

Cross-organ interactions between reproductive, gastrointestinal, and urinary tracts: modulation by estrous stage and involvement of the hypogastric nerve

Winnard¹,

Dmitrieva²,

Berkley³

2006

American Journal of Physiology-Regulatory, Integrative and Comp

101

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“…Also note that most of the neurons in the IML have reached a cytopathic stage; their profile is no longer clearly visible, unlike that of infected glia, which appear as small round black profiles. opt, thetic postganglionic fibers will cause and/or enhance plasma extravasation (Heller et al, 1994;Delepine and Aubineau, 1997). Still, little is known about the mechanisms by which the CNS could activate sensory or autonomic neurons to produce inflammation.…”

Section: Discussionmentioning

confidence: 99%

Activation for CNS Circuits Producing a Neurogenic Cystitis: Evidence for Centrally Induced Peripheral Inflammation

et al. 1999

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We present a model of neurogenic cystitis induced by viral infection of specific neuronal circuits of the rat CNS. Retrograde infection by pseudorabies virus (PRV) of neuronal populations neighboring those that innervate the bladder consistently led to a localized immune response in the CNS and bladder inflammation. Infection of bladder circuits themselves or of circuits distant from these rarely produced cystitis. Absence of virus in bladder and urine ruled out an infectious cystitis. Total denervation of the bladder, selective C-fiber deafferentation, or bladder sympathectomy prevented cystitis without affecting the CNS disease, indicating a neurogenic component to the inflammation. The integrity of central bladder-related circuits is necessary for the appearance of bladder inflammation, because only CNS lesions affecting bladder circuits, i.e., bilateral dorsolateral or ventrolateral funiculectomy, as well as bilateral lesions of Barrington's nucleus/locus coeruleus area, prevented bladder inflammation. The close proximity in the CNS of noninfected visceral circuits to infected somatic neurons would thus permit a bystander effect, leading to activation of the sensory and autonomic circuits innervating the bladder and resulting in a neurogenic inflammation localized to the bladder. The present study indicates that CNS dysfunction can bring about a peripheral inflammation.

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“…However, ACh released from SPG neurons can have untoward effects such as plasma protein extravasation in the dura mater and may lead to the release of proinflammatory and chemotactic proteins. This was demonstrated in a study that observed the mAChR-mediated neurogenic inflammation following electrical stimulation of rat SPG (Delepine and Aubineau 1997). Moreover, some forms of migraine and facial pain are associated with an enhanced parasympathetic activity.…”

Section: Discussionmentioning

confidence: 81%

Muscarinic Acetylcholine Receptor Modulation of Mu (μ) Opioid Receptors in Adult Rat Sphenopalatine Ganglion Neurons

Margas

Mahmoud

Ruiz‐Velasco

2010

Journal of Neurophysiology

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Margas W, Mahmoud S, Ruiz-Velasco V. Muscarinic acetylcholine receptor modulation of Mu () opioid receptors in adult rat sphenopalatine ganglion neurons. J Neurophysiol 103: 172-182, 2010. First published November 4, 2009 doi:10.1152/jn.00295.2009. The sphenopalatine ganglion (SPG) neurons represent the parasympathetic branch of the autonomic nervous system involved in controlling cerebral blood flow. In the present study, we examined the coupling mechanism between mu () opioid receptors (MOR) and muscarinic acetylcholine receptors (mAChR) with Ca 2ϩ channels in acutely dissociated adult rat SPG neurons. Successful MOR activation was recorded in ϳ40 -45% of SPG neurons employing the whole cell variant of the patch-clamp technique. In addition, immunofluorescence assays indicated that MOR are not expressed in all SPG neurons while M 2 mAChR staining was evident in all neurons. The concentration-response relationships generated with morphine and [d-Ala2-N-Me-Phe4-Glycol5]-enkephalin (DAMGO) showed IC 50 values of 15.2 and 56.1 nM and maximal Ca 2ϩ current inhibition of 26.0 and 38.7%, respectively. Activation of MOR or M 2 mAChR with morphine or oxotremorine-methiodide (Oxo-M), respectively, resulted in voltage-dependent inhibition of Ca 2ϩ currents via coupling with G␣ i/o protein subunits. The acute prolonged exposure (10 min) of neurons to morphine or Oxo-M led to the homologous desensitization of MOR and M 2 mAChR, respectively. The prolonged stimulation of M 2 mAChR with Oxo-M resulted in heterologous desensitization of morphine-mediated Ca 2ϩ current inhibition, and was sensitive to the M 2 mAChR blocker methoctramine. On the other hand, when the neurons were exposed to morphine or DAMGO for 10 min, heterologous desensitization of M 2 mAChR was not observed. These results suggest that in rat SPG neurons activation of M 2 mAChR likely modulates opioid transmission in the brain vasculature to adequately maintain cerebral blood flow.

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Plasma Protein Extravasation Induced in the Rat Dura Mater by Stimulation of the Parasympathetic Sphenopalatine Ganglion

Cited by 66 publications

References 37 publications

Cross-organ interactions between reproductive, gastrointestinal, and urinary tracts: modulation by estrous stage and involvement of the hypogastric nerve

Cross-organ interactions between reproductive, gastrointestinal, and urinary tracts: modulation by estrous stage and involvement of the hypogastric nerve

Activation for CNS Circuits Producing a Neurogenic Cystitis: Evidence for Centrally Induced Peripheral Inflammation

Muscarinic Acetylcholine Receptor Modulation of Mu (μ) Opioid Receptors in Adult Rat Sphenopalatine Ganglion Neurons

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