Enhancement of antral contractions and vagal afferent signaling with synchronized electrical stimulation.

Gastric filling activates vagal afferents involved in peripheral signaling to the central nervous system (CNS) for food intake. It is not known whether these afferents linearly encode increasing contractions of the antrum during antral distension (AD). The aim of this study was to investigate effects of AD and electrically enhanced antral contractions on responses of vagal afferents innervating the antrum. Single-fiber recordings were made from the vagal afferents in anesthetized male Long-Evans rats. Antral contractions were measured with a solid-state probe placed in the antrum. A nonexcitatory electrical stimulation (NES) inducing no smooth muscle contractions was applied during the ascending phase of antral contractions to enhance subsequent antral contractions. Fifty-six fibers identified during AD (1 ml for 30 s) were studied through different types of mechanical stimuli. Under normal conditions, one group of fibers exhibited rhythmic firing in phase with antral contractions. Another group of fibers had nonrhythmic spontaneous firing. Responses of 15 fibers were tested with NES during multiple-step distension (MSD). NES produced a mean increase in antral contraction amplitude (177.1 +/- 35.3%) and vagal afferent firing (21.6 +/- 2.6%). Results show that both passive distension and enhanced antral contractions activate distension-sensitive vagal afferents. Responses of these fibers increase linearly to enhanced antral contraction induced by NES or MSD up to a distending volume of 0.6 ml. However, responses reached a plateau at a distending volume >0.8 ml. We concluded that enhanced contraction of the antrum can activate vagal afferents signaling to the CNS.

[1]  S. Ben‐Haim,et al.  Cardiac Contractility Modulation With the Impulse Dynamics Signal: Studies in Dogs With Chronic Heart Failure , 2004, Heart Failure Reviews.

[2]  C. Pappone,et al.  Electrical Modulation of Cardiac Contractility: Clinical Aspects in Congestive Heart Failure , 2004, Heart Failure Reviews.

[3]  K. Ellison Nonexcitatory Stimulation: 2002: A Pace Odyssey , 2002, Journal of cardiovascular electrophysiology.

[4]  E. Fox,et al.  Selective loss of vagal intramuscular mechanoreceptors in mice mutant for steel factor, the c-Kit receptor ligand , 2002, Anatomy and Embryology.

[5]  D. Burkhoff,et al.  Cardiac contractility modulation by electric currents applied during the refractory period. , 2002, American journal of physiology. Heart and circulatory physiology.

[6]  J. D’Argent Gastric Electrical Stimulation as Therapy of Morbid Obesity: Preliminary Results from the French Study , 2002 .

[7]  J. D’Argent Gastric electrical stimulation as therapy of morbid obesity: preliminary results from the French study. , 2002, Obesity surgery.

[8]  E. Fox,et al.  Neurotrophin-4 Deficient Mice Have a Loss of Vagal Intraganglionic Mechanoreceptors from the Small Intestine and a Disruption of Short-Term Satiety , 2001, The Journal of Neuroscience.

[9]  D. Grundy,et al.  Somatostatin sst(2) receptor-mediated inhibition of mesenteric afferent nerves of the jejunum in the anesthetized rat. , 2001, Gastroenterology.

[10]  E. Fox,et al.  C-Kit mutant mice have a selective loss of vagal intramuscular mechanoreceptors in the forestomach , 2001, Anatomy and Embryology.

[11]  S. Brookes,et al.  Intraganglionic laminar endings are mechano‐transduction sites of vagal tension receptors in the guinea‐pig stomach , 2001, The Journal of physiology.

[12]  Terry L. Powley,et al.  Tension and stretch receptors in gastrointestinal smooth muscle: re-evaluating vagal mechanoreceptor electrophysiology , 2000, Brain Research Reviews.

[13]  T. Powley,et al.  Regenerating vagal afferents reinnervate gastrointestinal tract smooth muscle of the rat , 2000, The Journal of comparative neurology.

[14]  T. Powley,et al.  Topographic inventories of vagal afferents in gastrointestinal muscle , 2000, The Journal of comparative neurology.

[15]  D. Grundy,et al.  Modulation of gastrointestinal afferent sensitivity by a novel substituted benzamide (ecabapide). , 2000, Journal of the autonomic nervous system.

[16]  U. Ladabaum,et al.  Novel Approaches to the Treatment of Nausea and Vomiting , 1999, Digestive Diseases.

[17]  G. Gebhart,et al.  Mechanosensitive properties of gastric vagal afferent fibers in the rat. , 1999, Journal of neurophysiology.

[18]  G. P. Smith,et al.  Reduction of intake in the rat due to gastric filling. , 1997, The American journal of physiology.

[19]  H. Berthoud,et al.  Distribution and structure of vagal afferent intraganglionic laminar endings (IGLEs) in the rat gastrointestinal tract , 1997, Anatomy and Embryology.

[20]  T. Powley,et al.  Gastric volume rather than nutrient content inhibits food intake. , 1996, The American journal of physiology.

[21]  S. Ischia,et al.  Long-term Effects of Gastric Pacing to Reduce Feed Intake in Swine , 1996, Obesity surgery.

[22]  G. Gebhart,et al.  Characterization of mechanosensitive pelvic nerve afferent fibers innervating the colon of the rat. , 1994, Journal of neurophysiology.

[23]  P. McHugh,et al.  Integration of vagal afferent responses to gastric loads and cholecystokinin in rats. , 1991, The American journal of physiology.

[24]  G. Clarke,et al.  Mechanical properties and sensitivity to CCK of vagal gastric slowly adapting mechanoreceptors. , 1988, The American journal of physiology.

[25]  L. Blackshaw,et al.  Involvement of gastrointestinal mechano- and intestinal chemoreceptors in vagal reflexes: an electrophysiological study. , 1987, Journal of the autonomic nervous system.

[26]  R. McCallum Gastric emptying disorders. Tests and treatments. , 1987, Postgraduate medicine.

[27]  A. Rogers Gastric emptying disorders. , 1985, Comprehensive therapy.

[28]  J. Becker,et al.  Intestinal pacing for canine postgastrectomy dumping. , 1983, Gastroenterology.

[29]  D. Hopkins,et al.  The central distribution of the cervical vagus nerve and gastric afferent and efferent projections in the rat , 1982, Brain Research Bulletin.

[30]  J. A. Deutsch,et al.  Vagotomy abolishes cues of satiety produced by gastric distension. , 1981, Science.

[31]  P. Andrews,et al.  Vagal afferent discharge from mechanoreceptors in different regions of the ferret stomach. , 1980, The Journal of physiology.

[32]  P. Andrews,et al.  Reflex excitation of antral motility induced by gastric distension in the ferret. , 1980, The Journal of physiology.

[33]  G. Clarke,et al.  Tension receptors in the oesophagus and stomach of the rat. , 1975, The Journal of physiology.

[34]  T. Takeshima Functional Classification of Vagal Afferent Discharges in the Stomach of the Dog , 1974 .

[35]  T. Takeshima [Functional classification of the vagal afferent discharges in the dog's stomach]. , 1971, Nihon Heikatsukin Gakkai zasshi.

[36]  A. Iggo,et al.  Gastro-intestinal tension receptors with unmyelinated afferent fibres in the vagus of the cat. , 1957, Quarterly journal of experimental physiology and cognate medical sciences.

[37]  A. Paintal,et al.  A study of gastric stretch receptors. Their role in the peripheral mechanism of satiation of hunger and thirst , 1954, The Journal of physiology.