Parasympathetic and Sympathetic
Control of the Pancreas: A Role for the
Suprachiasmatic Nucleus and Other
Hypothalamic Centers That Are Involved
in the Regulation of Food Intake
RUUD M. BUIJS,
1
*
SOO JIN CHUN,
1,2
AKIRA NIIJIMA,
3
HERMS J. ROMIJN,
1
AND
KATSUYA NAGAI
2
1
Netherlands Institute for Brain Research, Meibergdreef 33,
Amsterdam 1105 AZ, The Netherlands
2
Division of Protein Metabolism, Institute for Protein Research, Osaka University,
3-2 Yamada-oka, Suita, Osaka 565-0871, Japan
3
Niigata University School of Medicine, Niigata, Niigata 951-8510, Japan
ABSTRACT
To reveal brain regions and transmitter systems involved in control of pancreatic hormone
secretion, specific vagal and sympathetic denervation were combined with injection of a retro-
grade transsynaptic tracer, pseudorabies virus (PRV), into the pancreas. After sympathetic or
vagal transsection first-order neurons were revealed in the dorsal motor nucleus of the vagus
(DMV) or in preganglionic spinal cord neurons (SPN), respectively. Careful timing of the survival
of the animals allowed the detection of cell groups in immediate control of these DMV or SPN
neurons. A far larger number of cell groups is involved in the control of DMV than of SPN
neurons. Examples are given of a high level of interaction between the sympathetic and para-
sympathetic nervous system. Several cell groups project to both branches of the autonomic
nervous system, sometimes even the same neurotransmitter is used, e.g., oxytocin neurons in the
paraventricular nucleus and melanin-concentrating hormone and orexin neurons in the lateral
hypothalamus project to both the DMV and SPN neurons. Moreover, the appearance of third-
order neurons located in the sympathetic SPN after complete sympathectomy and in the DMV
after complete vagotomy illustrates the possibility that motor neurons of the sympathetic and
parasympathetic system may exchange information by means of interneurons. The presence of
second-order neurons in prefrontal, gustatory, and piriform cortex may provide an anatomic basis
for the involvement of these cortices in the cephalic insulin response. The observation that
second-order neurons in both vagal and sympathetic control of the pancreas contain neuropep-
tides that are known to play a role in food intake indicates a direct association between behavioral
and autonomic functions. Finally, the observation of third-order neurons in the suprachiasmatic
nucleus and ventromedial hypothalamus shows the modulatory action of the time of the day and
metabolic state, respectively. J. Comp. Neurol. 431:405– 423, 2001. © 2001 Wiley-Liss, Inc.
Indexing terms: glucagon; paraventricular nucleus; prefrontal cortex; circadian rhythm
In mammals, the central nervous system (CNS) re-
quires glucose as an essential source of energy. Therefore,
to survive, mammals have to maintain their blood glucose
within a narrow range by means of central and peripheral
mechanisms (Oomura and Yoshimatsu, 1984; Choi et al.,
1996; Dallman et al., 1999). Blood glucose concentration
itself directly controls the secretion of the pancreatic hor-
mones insulin and glucagon. Not surprisingly, because of
the critical role glucose plays in the CNS, the brain also
affects insulin and glucagon release through the auto-
nomic nervous system (Frohman et al., 1967; Kaneto et
*Correspondence to: Ruud M. Buijs, Netherlands Institute for Brain
Research, Meibergdreef 33, Amsterdam 1105 AZ, The Netherlands.
E-mail: r.buijs@nih.knaw.nl
Received 17 July 2000; Revised 8 December 2000; Accepted 8 December
2000
THE JOURNAL OF COMPARATIVE NEUROLOGY 431:405– 423 (2001)
© 2001 WILEY-LISS, INC.