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The Journal of Neuroscience, October 25, 2006, 26(43):11052-11060; doi:10.1523/JNEUROSCI.2606-06.2006

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Behavioral/Systems/Cognitive
Gut Vagal Afferents Are Not Necessary for the Eating-Stimulatory Effect of Intraperitoneally Injected Ghrelin in the Rat

Myrtha Arnold,¹ Anna Mura,¹ Wolfgang Langhans,¹ and Nori Geary^1,2

¹Institute of Animal Sciences, Swiss Federal Institute of Technology Zurich, Schwerzenbach 8603, Switzerland, and ²Department of Psychiatry, Weill Medical College of Cornell University, New York, New York 10032

Correspondence should be addressed to Dr. Nori Geary, Institute of Animal Sciences, Swiss Federal Institute of Technology Zurich, Schwerzenbach 8603, Switzerland. Email: nori-geary{at}ethz.ch

Ghrelin is unique among gut peptides in that its plasma level increases during fasts and its administration stimulates eating. Although ghrelin physiology has been intensively studied, whether its eating-stimulatory effect arises from endocrine-neural signal transduction at peripheral or central sites remains unresolved. To address this issue, we tested the effects of subdiaphragmatic vagal deafferentation (SDA), the most complete and selective vagal deafferentation method available, on ghrelin-induced eating. SDA was verified with a cholecystokinin satiation test, retrograde labeling of vagal motor neurons in the dorsal motor nucleus of the vagus with fluorogold, and anterograde labeling of vagal afferents in the nucleus tractus solitarius with wheat germ agglutinin-horseradish peroxidase. Intraperitoneal injections of 10–40 µg/kg ghrelin stimulated eating as robustly in rats with verified complete SDA as in sham-operated controls. Ghrelin also stimulated eating in rats with total subdiaphragmatic vagotomies. We also recorded the electrophysiological responses of gastric load-sensitive vagal afferent neurons to intravenous ghrelin. Ghrelin (10 nmol) phasically (0–30 s) increased activity in two of seven gastric load-sensitive fibers in the absence of gastric loads and tonically (5–30 min) increased activity in only one fiber. Ghrelin did not affect any of the eight fibers tested in the presence of 1–3 ml gastric loads. We conclude that although phasic increases in plasma ghrelin may affect the activity of a fraction of gastric load-sensitive vagal afferents, the acute eating-stimulatory effect of intraperitoneal ghrelin does not require vagal afferent signaling.

Key words: food intake; obesity; vagus; electrophysiology; hunger; gastric mechanoreceptors

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Received June 21, 2006; revised Sept. 1, 2006; accepted Sept. 1, 2006.

Correspondence should be addressed to Dr. Nori Geary, Institute of Animal Sciences, Swiss Federal Institute of Technology Zurich, Schwerzenbach 8603, Switzerland. Email: nori-geary{at}ethz.ch

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