Neuroscience Research 67 (2010) 236–244
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Neuroscience Research
journal homepage: www.elsevier.com/locate/neures
Effect of an intraduodenal injection of fat on the activities of the adrenal efferent
sympathetic nerve and the gastric efferent parasympathetic nerve in
urethane-anesthetized rats
Shigenobu Matsumura
a,∗
, Ai Eguchi
a
, Nobuhide Kitabayashi
a
, Mamoru Tanida
b
, Jiao Shen
b
,
Yuko Horii
b
, Katsuya Nagai
b
, Satoshi Tsuzuki
a
, Kazuo Inoue
a
, Tohru Fushiki
a
a
Laboratory of Nutrition Chemistry, Division of Food Science and Biotechnology, Graduate School of Agriculture,
Kyoto University, Oiwake-cho, Kitashirakawa, Sakyo-ku, Kyoto 606-8502Japan
b
ANBAS Corporation, Japan
article info
Article history:
Received 9 July 2009
Received in revised form 24 March 2010
Accepted 25 March 2010
Available online 31 March 2010
Keywords:
Fat
Autonomic nerve
Adrenal efferent sympathetic nerve
Gastric efferent parasympathetic nerve
Fatty acid
abstract
Nutrient information from the gastrointestinal tract to the brain plays a critical role in the regulation
of appetite and energy homeostasis. The autonomic nervous system controls the functions of several
tissues to regulate the energy homeostasis of the whole body. Autonomic nerve activity is influenced by
environmental or exogenous changes in even a single tissue. In the present study, we investigated the
effect of an intraduodenal injection of fat on the activities of the autonomic nerves innervating the adrenal
gland and stomach in urethane-anesthetized rats. An intraduodenal injection of corn oil suppressed
adrenal efferent sympathetic nerve activity (ASNA) and stimulated gastric efferent vagal nerve activity
(GVNA). A lipase inhibitor, -polylysine, coinjected with corn oil completely suppressed the corn oil-
induced changes in ASNA and GVNA. Further, an intraduodenal injection of fatty acid (linoleic acid)
moderately suppressed ASNA and significantly stimulated GVNA; these results indicate that fat may affect
autonomic nerve activity partly through the chemoreception of free fatty acids (FFAs), which are produced
during the hydrolysis of fat (corn oil) by a pancreatic lipase, in the intestinal lumen. Furthermore, an
intraduodenal injection of an intravenous fat emulsion with the same pH and osmotic pressure as the body
fluid affected ASNA and GVNA in a similar manner as corn oil. These results suggest that intraduodenal fat
suppresses ASNA and stimulates GVNA partly via the chemoreception of FFAs—the degradation products
of fats—in the intestinal lumen.
© 2010 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved.
1. Introduction
Fatty foods are satiable and generally more palatable to humans
than low-calorie or low-fat foods. This preference for fatty foods is
also observed in mice and rats (Ackroff et al., 1990; Tsuruta et al.,
1999; Imaizumi et al., 2000, 2001; Fukuwatari et al., 2003). Animals
prefer dietary fats for survival because fats are a good source of
energy for the body.
The gastrointestinal tract and the vagus nerve that innervates
the visceral organs regulate the volume and profile of luminal
nutrients (Janig, 1996; Schwartz, 2000; Raybould, 2002). When
the ingested food reaches the upper intestine, various kinds of
physiological responses are elicited for digestion and absorption.
The ingested fat itself promotes these responses for more effi-
cient fat absorption and metabolism. For example, fat promotes the
∗
Corresponding author. Tel.: +81 75 753 6263; fax: +81 75 753 6264.
E-mail address: sigenobu@kais.kyoto-u.ac.jp (S. Matsumura).
secretion of gastrointestinal hormones from enteroendocrine cells.
These hormones stimulate the secretion of gastric acid, digestive
enzymes, or bile acid and modulate gastric emptying or gastroin-
testinal motility. Further, results of recent studies have suggested
that ghrelin, cholecystokinin (CCK), glucagon-like peptide-1 (GLP-
1), and peptide YY significantly influence the regulation of food
intake and energy homeostasis (Imeryuz et al., 1997; Challis et al.,
2003; Peters et al., 2006; Berthoud, 2008). The hormonal signals are
detected in and integrated with specific regions of the brain, such
as the hypothalamus and brain stem.
In addition to hormonal signals, the gastrointestinal tract trans-
mits signals of ingested fat to the brain via the vagus nerve. Randich
and coworkers have reported that injection of triacylglycerides
(TGs) or free fatty acids (FFAs) into the intestine stimulates the
afferent vagal nerve or the hepatic branch of the vagus nerve
(Randich et al., 2000; Randich et al., 2001). Moreover, it has been
reported that subdiaphragmatic vagotomy and selective celiac
vagotomy attenuate the suppression of food intake induced by jeju-
nal infusion of linoleic acid or corn oil (Yox et al., 1991; Walls
0168-0102/$ – see front matter © 2010 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved.
doi:10.1016/j.neures.2010.03.010