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Neural and Hormonal Control of Gastric Secretion

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Abstract

The sections in this article are:

1 Central Controls
1.1 Central Vagal Complex
1.2 Functional Anatomy of the Vagal Complex
1.3 Brain Peptides Relating to Gastric Secretion
1.4 Vagal Excitation by Glucoprivation
1.5 Non‐Glucose‐Related Chemical Stimuli of the Central Vagus
1.6 Vagal Afferents
2 Peripheral Controls of Gastric Secretion
2.1 Enteric Nervous System
2.2 Chemical Transmitters of Neural Effects
2.3 Trophic Effects
2.4 Antrofundal Interactions
2.5 Vagotomy
2.6 Intestinal Phase of Gastric Secretion
Figure 1. Figure 1.

A: schematic transverse section of the medulla showing its basic features. Cell columns related to functional components of the cranial nerve are indicated on the right. Functional components of cranial nerves are both general and special. Functional components of the vagus nerve are shown in relation to particular nuclei. Heavy dashes separate nuclei of the various cell columns on the right. B: schematic illustration of the connections of the central vagal complex. DMNV, dorsomotor nucleus of the vagus; gsa, general somatic afferents; gse, general somatic efferents; gva, general visceral afferents; gve, general vagal efferents; INF VG, inferior vagal ganglion; LH, lateral hypothalamus; MFB, median forebrain bundle; NA, nucleus ambiguus; NTS, nucleus tractus solitarius; NX, vagus nerve; PVN, paraventricular nucleus; SSA, special somatic afferents; SUP VG, superior vagal ganglion; SVA, special visceral afferent; SVE, special visceral efferents; TS, tractus solitarius; VMH, ventromedian hypothalamus. Sites stimulated by glucoprivation: LH, MFB, NTS, NA.

A from Carpenter
Figure 2. Figure 2.

Mechanism of action of glucose analogues in causing cerebral glucoprivation at sites that act via the dorsomotor nucleus of the vagus (DMNV). 2‐DG, 2‐deoxy‐d‐glucose; 2DG‐6‐P, 2‐deoxy‐d‐glucose‐6‐phosphate; 3‐O‐MG, 3‐O‐methylglucose; HMP, hexose monophosphate.

Figure 3. Figure 3.

Acid and pepsin outputs in gastric fistula dogs with intact vagi given 2‐DG, 100 μg/kg iv over 30 min. VH, acid output; VP, pepsin output.

From Hirschowitz and Sachs
Figure 4. Figure 4.

Responses to vagal stimulation are dose or stimulus dependent. Acid (H) and pepsin (P) related to electrical stimulation of vagal trunks ; pepsin secretion related to the level of blood sugar ; gastrin release and acid secretion and antral motility related to dose of 2‐deoxy‐d‐glucose.

From Hirschowitz
Figure 5. Figure 5.

Secretion of acid and pepsin in the basal state min) during and after 15‐min modified sham feeding (MSF) – min) and after pentagastrin 6 μg/kg subcutaneously in 4 groups of subjects. Duodenal ulcer (DU) (n = 60), normal controls (n = 40), duodenal ulcer after fundic vagotomy (Vag) (n = 20), and duodenal ulcer after truncal vagotomy and antrectomy (Ant) (n = 16). n, Number of subjects.

Figure 6. Figure 6.

Schematic drawing of autonomic innervation of the stomach by vagal and adrenergic neurons. A, afferent; E, endocrine (shown as both open and closed cells); G, ganglia; P, paracrine; S, secretory cells.

Figure 7. Figure 7.

Paracrine controls of gastric secretion include possible stimulatory release of histamine (HIST) from a tissue histamine cell by acetylcholine (ACh) and perhaps gastrin (G). Inhibitory effects of somatostatin may involve both gastrin and parietal (PAR) cells. Undefined paracrine effects include unknown parietal‐peptic cell interactions via gap junctions. Middle panel, both open (antral) and closed (fundus) G and D cells are shown. D, D cells; SOM, somatostatin; (‐), inhibition.

Figure 8. Figure 8.

Major factors controlling release of gastrin by the vagus. Negative feedback inhibiting gastrin release may act directly via acid in the lumen on the open end of the gastrin cell (G cell); both H+ and acetylcholine (ACh) may act by releasing somatostatin (SOM). BB, bombesin; (+), stimulation; (–), inhibition. Interpretation from results of studies in intact animals.

Figure 9. Figure 9.

Effects of an intravenous injection of 2‐DG on acid and pepsin output during a continuous infusion of histamine. In another experiment, 2‐DG was given with atropine, 80 μg/kg. PU, peptic unit.

From Hirschowitz and Sachs
Figure 10. Figure 10.

Acid output in fistula dogs related to measured concentrations of serum gastrin. Dogs were stimulated by graded doses – μg·kg‐1·h‐1) of bethanechol (BCh), bombesin (.1‐2 μg·kg‐1·h‐1), and gastrin G‐17 (.05‐5 μg·kg‐1·h‐1). Inset: bethanechol dose response in 3 dogs before (intact) and after fundic vagotomy (Vagot).

Figure 11. Figure 11.

Change in serum gastrin in the 4 h after intravenous injection of 2‐DG, 100 mg/kg, in 4 dogs before and 1 and 4 mo after antral vagotomy. FSG, fasting serum gastrin.

Figure 12. Figure 12.

Effect of atropine on serum gastrin after an injection of 2‐DG, 100 μg/kg, given intravenously over a 10‐min period with or without atropine. Studies were performed in conscious fistula dogs before (intact) and after highly selective (fundic) vagotomy (HSV).

Figure 13. Figure 13.

Gastric acid response to graded doses of pentagastrin (left panel) and serum gastrin response to 2‐DG (right panel) in 3 dogs before and after fundic vagotomy. After fundic vagotomy, bethanechol (Urecholine), 10 μg·kg‐1·h‐1 was given as background (Post + UCh).

From Hirschowitz
Figure 14. Figure 14.

Acidification of antrum to pH <1.4 in fistula dogs inhibited gastrin release by 2‐DG with intact vagi (A), 2‐DG after fundic vagotomy (B), a meal of 350‐g meat (C), but not bombesin nonapeptide (D).

Figure 15. Figure 15.

Top: summary of the integrated acid and gastrin output in response to intravenous 2‐DG stimulation in dogs with intact vagi and after fundic, truncal, and antral vagotomy. HSV, highly selective (fundic) vagotomy; TV, truncal vagotomy; AV, antral vagotomy; IGR, integrated gastrin response. Shading, vagally denervated parts of the stomach. Bottom: acid and gastrin responses to 3‐h intravenous infusion of bombesin‐14 in 3 dogs before and after fundic and subsequent truncal vagotomy. In the fundic vagotomy experiments, the effect of a background of bethanechol [Urecholine (UCh), 10 μg·kg‐1·h‐1] on acid and gastrin are shown.

From Hirschowitz
Figure 16. Figure 16.

Acid output and gastrin release with 2‐DG in dogs before (intact) and after highly selective (fundic) vagotomy (HSV). In the same dogs, subsequent truncal vagotomy (TV) eliminated both acid and gastrin responses.

From Hirschowitz
Figure 17. Figure 17.

Effect of fundic (highly selective) vagotomy on acid and pepsin responses to 2‐DG, 100 μ/kg, before and 1, 6, 9, and 12 mo later. Right panel, acid responses to graded doses of bethanechol Urecholine) before and up to 14 mo after vagotomy.

Adapted from Hirschowitz and Hutchison .
Figure 18. Figure 18.

Acid and pepsin output in response to 100 mg/kg 2‐DG (top) remained substantially unaltered by antral vagotomy (AV) in 4 dogs. Response to pentagastrin (bottom left) was reduced; response to bethanechol (lower right) was increased by antral vagotomy.



Figure 1.

A: schematic transverse section of the medulla showing its basic features. Cell columns related to functional components of the cranial nerve are indicated on the right. Functional components of cranial nerves are both general and special. Functional components of the vagus nerve are shown in relation to particular nuclei. Heavy dashes separate nuclei of the various cell columns on the right. B: schematic illustration of the connections of the central vagal complex. DMNV, dorsomotor nucleus of the vagus; gsa, general somatic afferents; gse, general somatic efferents; gva, general visceral afferents; gve, general vagal efferents; INF VG, inferior vagal ganglion; LH, lateral hypothalamus; MFB, median forebrain bundle; NA, nucleus ambiguus; NTS, nucleus tractus solitarius; NX, vagus nerve; PVN, paraventricular nucleus; SSA, special somatic afferents; SUP VG, superior vagal ganglion; SVA, special visceral afferent; SVE, special visceral efferents; TS, tractus solitarius; VMH, ventromedian hypothalamus. Sites stimulated by glucoprivation: LH, MFB, NTS, NA.

A from Carpenter


Figure 2.

Mechanism of action of glucose analogues in causing cerebral glucoprivation at sites that act via the dorsomotor nucleus of the vagus (DMNV). 2‐DG, 2‐deoxy‐d‐glucose; 2DG‐6‐P, 2‐deoxy‐d‐glucose‐6‐phosphate; 3‐O‐MG, 3‐O‐methylglucose; HMP, hexose monophosphate.



Figure 3.

Acid and pepsin outputs in gastric fistula dogs with intact vagi given 2‐DG, 100 μg/kg iv over 30 min. VH, acid output; VP, pepsin output.

From Hirschowitz and Sachs


Figure 4.

Responses to vagal stimulation are dose or stimulus dependent. Acid (H) and pepsin (P) related to electrical stimulation of vagal trunks ; pepsin secretion related to the level of blood sugar ; gastrin release and acid secretion and antral motility related to dose of 2‐deoxy‐d‐glucose.

From Hirschowitz


Figure 5.

Secretion of acid and pepsin in the basal state min) during and after 15‐min modified sham feeding (MSF) – min) and after pentagastrin 6 μg/kg subcutaneously in 4 groups of subjects. Duodenal ulcer (DU) (n = 60), normal controls (n = 40), duodenal ulcer after fundic vagotomy (Vag) (n = 20), and duodenal ulcer after truncal vagotomy and antrectomy (Ant) (n = 16). n, Number of subjects.



Figure 6.

Schematic drawing of autonomic innervation of the stomach by vagal and adrenergic neurons. A, afferent; E, endocrine (shown as both open and closed cells); G, ganglia; P, paracrine; S, secretory cells.



Figure 7.

Paracrine controls of gastric secretion include possible stimulatory release of histamine (HIST) from a tissue histamine cell by acetylcholine (ACh) and perhaps gastrin (G). Inhibitory effects of somatostatin may involve both gastrin and parietal (PAR) cells. Undefined paracrine effects include unknown parietal‐peptic cell interactions via gap junctions. Middle panel, both open (antral) and closed (fundus) G and D cells are shown. D, D cells; SOM, somatostatin; (‐), inhibition.



Figure 8.

Major factors controlling release of gastrin by the vagus. Negative feedback inhibiting gastrin release may act directly via acid in the lumen on the open end of the gastrin cell (G cell); both H+ and acetylcholine (ACh) may act by releasing somatostatin (SOM). BB, bombesin; (+), stimulation; (–), inhibition. Interpretation from results of studies in intact animals.



Figure 9.

Effects of an intravenous injection of 2‐DG on acid and pepsin output during a continuous infusion of histamine. In another experiment, 2‐DG was given with atropine, 80 μg/kg. PU, peptic unit.

From Hirschowitz and Sachs


Figure 10.

Acid output in fistula dogs related to measured concentrations of serum gastrin. Dogs were stimulated by graded doses – μg·kg‐1·h‐1) of bethanechol (BCh), bombesin (.1‐2 μg·kg‐1·h‐1), and gastrin G‐17 (.05‐5 μg·kg‐1·h‐1). Inset: bethanechol dose response in 3 dogs before (intact) and after fundic vagotomy (Vagot).



Figure 11.

Change in serum gastrin in the 4 h after intravenous injection of 2‐DG, 100 mg/kg, in 4 dogs before and 1 and 4 mo after antral vagotomy. FSG, fasting serum gastrin.



Figure 12.

Effect of atropine on serum gastrin after an injection of 2‐DG, 100 μg/kg, given intravenously over a 10‐min period with or without atropine. Studies were performed in conscious fistula dogs before (intact) and after highly selective (fundic) vagotomy (HSV).



Figure 13.

Gastric acid response to graded doses of pentagastrin (left panel) and serum gastrin response to 2‐DG (right panel) in 3 dogs before and after fundic vagotomy. After fundic vagotomy, bethanechol (Urecholine), 10 μg·kg‐1·h‐1 was given as background (Post + UCh).

From Hirschowitz


Figure 14.

Acidification of antrum to pH <1.4 in fistula dogs inhibited gastrin release by 2‐DG with intact vagi (A), 2‐DG after fundic vagotomy (B), a meal of 350‐g meat (C), but not bombesin nonapeptide (D).



Figure 15.

Top: summary of the integrated acid and gastrin output in response to intravenous 2‐DG stimulation in dogs with intact vagi and after fundic, truncal, and antral vagotomy. HSV, highly selective (fundic) vagotomy; TV, truncal vagotomy; AV, antral vagotomy; IGR, integrated gastrin response. Shading, vagally denervated parts of the stomach. Bottom: acid and gastrin responses to 3‐h intravenous infusion of bombesin‐14 in 3 dogs before and after fundic and subsequent truncal vagotomy. In the fundic vagotomy experiments, the effect of a background of bethanechol [Urecholine (UCh), 10 μg·kg‐1·h‐1] on acid and gastrin are shown.

From Hirschowitz


Figure 16.

Acid output and gastrin release with 2‐DG in dogs before (intact) and after highly selective (fundic) vagotomy (HSV). In the same dogs, subsequent truncal vagotomy (TV) eliminated both acid and gastrin responses.

From Hirschowitz


Figure 17.

Effect of fundic (highly selective) vagotomy on acid and pepsin responses to 2‐DG, 100 μ/kg, before and 1, 6, 9, and 12 mo later. Right panel, acid responses to graded doses of bethanechol Urecholine) before and up to 14 mo after vagotomy.

Adapted from Hirschowitz and Hutchison .


Figure 18.

Acid and pepsin output in response to 100 mg/kg 2‐DG (top) remained substantially unaltered by antral vagotomy (AV) in 4 dogs. Response to pentagastrin (bottom left) was reduced; response to bethanechol (lower right) was increased by antral vagotomy.

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Basil I. Hirschowitz. Neural and Hormonal Control of Gastric Secretion. Compr Physiol 2011, Supplement 18: Handbook of Physiology, The Gastrointestinal System, Salivary, Gastric, Pancreatic, and Hepatobiliary Secretion: 127-157. First published in print 1989. doi: 10.1002/cphy.cp060308