Sources of anterior gastric vagal efferent discharge in rats: an electrophysiological study

ArticleinJournal of the Autonomic Nervous System 37(1):29-37 · February 1992with4 Reads
DOI: 10.1016/0165-1838(92)90142-4 · Source: PubMed
Abstract
The source of vagal efferent discharge (VED) in the anterior branch of the gastric vagus was investigated in urethane-chloralose anesthetized rats using successive and selective vagal cuts. After cutting the right cervical vagus, the basal VEDs were increased in 15 out of 21 cases by 4-53% (median 18%). After both cervical vagi were cut, VEDs were reduced by 10-95% (median 90%) in 14 of 17 experiments and a subcervical basal VED was observed in all rats. Additional cut of the distal end of the anterior gastric branch did not induce a consistent effect. A small segment of subdiaphragmatic anterior gastric vagus (4-5 mm) was further isolated by a fourth cut at the proximal end of the anterior gastric vagus; abolition of the subcervical VED occurred in only 4 of 14 successful cuts whereas in the other 10 experiments, the VED was reduced by 38-94% (median 87%). Histological examination revealed the presence of neurons in a paraganglion lying within the isolated nerve segment. These findings indicate that the stomach not only receives VED descending directly from medullary vagal motor neurons (about 90%), but also (approximately 10%) from neural elements located between subcervical to upper abdomen levels (the 'subcervical VED') and/or between the bifurcation of the accessory celiac branch to the gastro-esophageal junction (the 'residual VED'). In rats there is little crossed gastric vagal innervation, in agreement with anatomical observations, although there is a robust inhibitory influence from contralateral vagal afferents on medullary vagal motor neurons.
    • Finally, centrifugally directed CCK-8-evoked impulse activity might be the result of descending impulse traffic in axon collaterals of afferent fibres innervating both the oesophagus and stomach. It has previously been shown that approximately 10% of centrifugal impulse activity recorded in the VGV is attributable to activity in axon collaterals with this type of branching (Wei et al. 1992Wei et al. , 1995). The diversity of efferent response types within each branch are consistent with work in the ferret demonstrating that both proximal and distal regions of the stomach each receive a combination of excitatory and inhibitory vagal motor inputs (Andrews & Scratcherd, 1980), and provides support for earlier proposals, based on recordings of efferent activity made at the cervical level, that gastric smooth muscle activity in each region is adjusted by reciprocal changes in excitatory and inhibitory drive (Grundy et al. 1981; Blackshaw & Grundy, 1989; Chang et al. 2003).
    [Show abstract] [Hide abstract] ABSTRACT: Gut activity is controlled by the vagus nerves. In anaesthetized rats, both sensory and motor nerve activity evoked by intravenous injection of the gut hormone cholecystokinin were recorded in separate sub-branches of the gastric vagus nerve that supply the forestomach and hindstomach, respectively. Activity in the forestomach branch has not been studied before. Motor nerve activity in response to cholecystokinin differed between the two branches, in both timing and direction. Motor output to the forestomach paralleled sensory input from the hindstomach, while motor output to the hindstomach paralleled sensory input from the intestines. The data suggest that cholecystokinin released in the intestines after a meal immediately influences churning and propulsion of food by the hindstomach, via reflexes initiated by nearby intestinal sensory nerve terminals, but may influence gastric capacity only later, once circulating levels of cholecystokinin rise to levels capable of activating sensors in the hindstomach. Abstract Intravenous cholecystokinin octapeptide (CCK-8) elicits vago-vagal reflexes that inhibit phasic gastric contractions and reduce gastric tone in urethane-anaesthetized rats. A discrete proximal subdivision of the ventral gastric vagus nerve (pVGV) innervates the proximal stomach, but the fibre populations within it have not been characterized previously. We hypothesized that i.v. CCK-8 injection would excite inhibitory efferent outflow in the pVGV, in contrast to its inhibitory effect on excitatory efferent outflow in the distal subdivision (dVGV), which supplies the distal stomach. In each VGV subdivision, a dual-recording technique was used to record afferent and efferent activity simultaneously, while also monitoring intragastric pressure (IGP). CCK-8 dose dependently (100–1000 pmol kg−1, i.v.) reduced gastric tone, gastric contractile activity and multi-unit dVGV efferent discharge, but increased pVGV efferent firing. Single-unit analysis revealed a minority of efferent fibres in each branch whose response differed in direction from the bulk response. Unexpectedly, efferent excitation in the pVGV was significantly shorter lived and had a significantly shorter decay half-time than did efferent inhibition in the dVGV, indicating that distinct pathways drive CCK-evoked outflow to the proximal vs. the distal stomach. Efferent inhibition in the dVGV began several seconds before, and persisted significantly longer than, simultaneously recorded dVGV afferent excitation. Thus, dVGV afferent excitation could not account for the pattern of dVGV efferent inhibition. However, the time course of dVGV afferent excitation paralleled that of pVGV efferent excitation. Similarly, the duration of CCK-8-evoked afferent responses recorded in the accessory celiac branch of the vagus (ACV) matched the duration of dVGV efferent responses. The observed temporal relationships suggest that postprandial effects on gastric complicance of CCK released from intestinal endocrine cells may require circulating concentrations to rise to levels capable of exciting distal gastric afferent fibres, in contrast to more immediate effects on distal gastric contractile activity mediated via vago-vagal reflexes initiated by paracrine excitation of intestinal afferents.
    Full-text · Article · Nov 2010
    • On the other hand, the gastric afferents are much more complex. Although sensory fibers from the stomach run through the greater splanchnic nerves and enter the spinal cord around T 7 T 9 , the vagi nerves also carry sensory fibers both in rats and humans (Wei et al., 1992). The pathophysiology of AD is complex.
    [Show abstract] [Hide abstract] ABSTRACT: Upper gastrointestinal (GI) motility inhibition after spinal cord injury has been classically considered to result from autonomic dysreflexia (AD). Animal models have been designed in rats to evaluate the presence of AD induced by colonic or bladder distension. However, there are no animal models of AD induced by gastric distension (GD). We examined whether controlled GD could induce AD and compared the pattern of hemodynamic responses induced by GD with colonic distensions (CD) and the interaction between them. Male Wistar rats underwent spinal cord transections performed at the level of C(7)-T(1), T(4)-T(5) and T(9)-T(10) (control) vertebrae and the presence of AD was evaluated after 1 day. In animals with C(7)-T(1) lesions, each CD in a series of 4 consecutive CDs triggered AD while GD only triggered AD after the 2 initial distensions in a series of 4 consecutive GDs. In animals with T(4)-T(5) lesions, in a protocol of 4 consecutive CDs or GDs, AD was triggered only by the 2 initial distensions. In 2 other protocols, consisting of 2 consecutive CDs or GDs followed respectively by 2 GDs or CDs, the effect of 2 GDs was attenuated in animals with C(7)-T(1) and T(4)-T(5) lesions but the hemodynamic changes induced by CDs were not affected by prior GDs. In summary, this is a new model of AD triggered by GD in rats. AD is more intense in animals with C(7)-T(1) lesions than after T(4)-T(5) lesions and AD triggered by GD can be attenuated by prior CDs.
    Full-text · Article · Sep 2008
    • Less than 5% of the gastric DMN projection in the VGV is nitrergic (Hyland et al. 2001; Zheng et al. 1999). An estimated 10% of descending impulse activity in the VGV originates from subcervical sources (Wei et al. 1992), which include vagal paraganglion cells (Prechtl and Powley 1985, 1990 ), descending axon collaterals of afferent fibers (Wei et al. 1992Wei et al. , 1995), and a small number of catecholaminergic sympathetic efferent fibers (Yang et al. 1999). Given the large proportion of fibers inhibited by iv CRF, coupled with the predominance of cholinergic vagal motor fibers, it seems likely that the great majority of VE fibers inhibited by iv CRF comprised cholinergic neurons of the excitatory pathway to the hindstomach.
    [Show abstract] [Hide abstract] ABSTRACT: Corticotropin-releasing factor (CRF) injected peripherally or released in response to stressful challenges to the organism reduces gastric tone and contractility, in part by vagal pathways. However, information on the changes in gastric vagal impulse activity evoked by peripheral CRF administration is entirely lacking. Using a novel "dual recording" method in urethane-anesthetized rats, vagal efferent (VE) and afferent (VA) impulse activities were recorded simultaneously from separate, fine bundles dissected from the ventral gastric vagus nerve branch innervating the glandular stomach. Activity records for 38 VA single units (SUs) and 33 VE SUs were sorted from multiunit records obtained from 13 preparations. Intravenous (iv) administration of saline had no effect on multiunit VE activity, whereas CRF (1 microg/kg, iv) immediately inhibited VE activity, reaching a nadir of 54 +/- 8.0% of preinjection levels at 3.0 min postinjection. CRF (1 microg/kg, iv) inhibited 25/33 (75.8%) VE SUs and excited three of 33 (9.1%) VE SUs. In contrast to potent effects on VE activity, iv CRF did not alter multiunit VA activity. Single-unit analysis, however, revealed five of 38 (13.1%) VA SUs excited by iv CRF at widely varying latencies (suggesting an indirect mode of action) and one inhibited VA SU. VA SUs excited after iv CRF did not respond during gastric distention and vice versa. These experiments are the first to use simultaneous recording of gastric VA and VE units. The data demonstrate a predominantly inhibitory influence of iv CRF on VE outflow to the hindstomach, not driven by gastric vagovagal reflex activity.
    Full-text · Article · May 2007
  • [Show abstract] [Hide abstract] ABSTRACT: There is convincing electrophysiological, neuroanatomical and functional data in support of an excitatory action of thyrotropin-releasing hormone (TRH) on the dorsal motor nucleus of the vagus neurons leading to stimulation of vagal outflow to the stomach and to a vagal cholinergic-dependent stimulation of gastric secretory and motor function and alterations of mucosal integrity in rats and cats. The raphe pallidus and obscurus have become important medullary nuclei regulating vagal function through their TRH and serotonin projections to the dorsal vagal complex. However, still little is known about the transmitters and conditions which influence the activity of these TRH-containing medullary raphe neurons. Existing knowledge points out a possible physiological role of TRH in mediating vagal reflex and the cephalic phase of digestion.
    Article · Feb 1993
  • [Show abstract] [Hide abstract] ABSTRACT: The central nervous system action of bombesin to influence basal gastric vagal efferent discharge (GVED) was investigated in urethane-anesthetized rats. Bombesin (62, 620, and 6200 pmol) injected intracisternally (IC) decreased GVED to 78 +/- 10%, 50 +/- 4%, and 43 +/- 3% of preinjection levels, respectively. Bombesin (620 pmol) injected IV also reduced GVED to 36 +/- 6%. Pretreatment with bombesin monoclonal antibody 2A11 completely prevented the decrease in GVED induced by bombesin (620 pmol) given IV but not IC. These data indicate that both IC and IV injections of bombesin decrease basal GVED, and that the inhibitory effect of IC injection represents a central nervous system-mediated action.
    Article · Mar 1993
  • [Show abstract] [Hide abstract] ABSTRACT: The influence of intravenous (iv) bombesin on multiunit activities recorded from the ventral gastric branch of the vagus was investigated in urethan-anesthetized rats. Consecutive injections of bombesin (0.062, 0.62, 6.2, 62, and 620 pmol iv) decreased dose dependently gastric vagal efferent discharges to 79.8 +/- 4.9, 68.3 +/- 10.2, 47.0 +/- 6.7, 41.6 +/- 4.7, and 36.5 +/- 8.9%, respectively, from preinjection levels. Saline injection had no effect. Bombesin (62 pmol iv) reduced cervical vagal efferent discharges to 25 +/- 6% before and 67 +/- 5% after bilateral cervical vagotomy distal to the recording site. Bombesin (62 and 620 pmol iv) increased gastric vagal afferent discharges by 45 and 93%, respectively. These data show that systemic injection of bombesin potently decreases gastric and cervical vagal efferent activity in part through vagal-dependent mechanisms that may involve the increase in gastric vagal afferent activity.
    Article · Jul 1994
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