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Brain Research Bulletin, Vol. 26, pp. 165-167. Q Pergamon Press plc, 1991. Printed in the U.S.A

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Effects of Taste Stimulation on the Efferent Activity of the Autonomic Nerves in the Rat’ AKIRA NIIJIMA Department of Physiology, Niigata University School of Medicine, Niigata 951, Japan Received

5 July 1990

NIIJIMA, A. Effects of taste stimulation on the efferent activity of the autonomic nerves in the rat. BRAIN RES BULL 26( 1) 165167, 1991. -Effects of taste stimulation on the efferent discharges in the pancreatic and hepatic branch of the vagus nerve, and those in the adrenal, pancreatic and hepatic branch of the splanchnic nerve, and the sympathetic nerve innervating interscapular brown adipose tissue, were observed in the anesthetized rat. Sweet taste stimulation with 5% glucose or 10% sucrose caused an increase in activity of pancreatic and hepatic branch of the vagus nerve and brown adipose tissue nerve, and a decrease in discharge rate of the adrenal, pancreatic and hepatic branch of the splanchnic nerve. Salty taste stimulation with 5% NaCl resulted in opposite effects in these nerves. Results suggest preabsorptive reflex control of visceral functions due to taste stimulation. Taste stimulus

Reflex

Autonomic

nerve

Pancreas

Liver

Adrenal medulla

Brown adipose tissue

thetized with urethane (700 mg/kg) and chloralose (50 mg/kg) (IP). A trachea cannula was inserted. Small nerve bundles were dissected from the pancreatic or hepatic branch of the vagus nerve, and from the adrenal, pancreatic or hepatic branch of the splanchnit nerve. Small nerve bundles were also dissected from the nerve branches innervating the right side of interscapular brown adipose tissue. Under a dissecting microscope, nerve filaments were isolated from the central cut end of these nerve bundles to record the efferent activity with a pair of silver wire electrodes. Nerve activity was amplified and displayed on an oscilloscope and stored on magnetic tape. A rate meter with a reset time of 5 s was used to observe the time course of the nerve activity that was recorded with a pen recorder. Animal body temperature was maintained by means of a heating pad. For sweet taste stimulation 5% glucose solution or 10% sucrose solution was used. Five percent NaCl solution was used as a strong salty taste stimulation. These solutions were applied to the tongue surface with a syringe. Each trial required 2 or 5 min to spread the solution over the tongue at rate of 0.8-l .O mYmin, and the tongue was flushed with distilled water at the end of each taste stimulation.

IT was reported

by Niijima (5) in 1979 that sweet taste stimulation increased efferent activity of the pancreatic vagus nerve in anesthetized rat. He further observed that there was not only an increase in discharge rate following sweet taste stimulation with 10% sucrose solution but also a decrease by a strong salty taste stimulation with 5% NaCl solution in normal as well as decerebrated rat (6). His observations suggest the existence of a gustatory vago-pancreatic reflex system which may control the function of the endocrine pancreas. It is also possible to assume that the gustatory input plays a more general role in control of the function of several visceral organs such as pancreas, liver and adrenal medulla through gustatory-vagal and gustatory-sympathetic reflex pathways. This paper mainly deals with the preliminary work on the effects of taste stimulation on the rate of efferent discharges in the pancreatic and hepatic branch of the vagus nerve, and in the adrenal, pancreatic and hepatic branch of the splanchnic nerve. The effect of the activity of the sympathetic nerve innervating interscapular brown adipose tissue was also investigated. METHOD

RESULTS

Wister rats weighing about 300 g were used. Animals had free access to food and water before the experiment. Rats were anes-

It has already been reported

that sweet taste stimulation

with

‘This article was presented at the Xth International Congress on the Physiology of Food and Fluid Intake held in Paris, France, July 4-8, 1989. Other selected articles from this meeting have been published in Physiology & Behavior, Volume 48, Number 6, 1990, Volume 49, Number 1, 1991 and Brain Research Bulletin, Volume 25, Number 6, 1990.

165

NIIJIMA

166

5% Glucose

5% Glucose

5 min

10% Sucrose

5% NaCl

5% Glucose

5% NaCl 5% NaCl

5% Glucose 50

2

2 0I

Smi”

10% Sucrose

5%- NaCl

100

RG. 1. Effects of taste stimulation on the efferent activity of pancreatic branch (upper trace) and hepatic branch (lower trace) of the vagus nerve in the rat. Vertical bars, 100 impulses per 5 s.

10% glucose for 5 min caused an activation of efferent discharges in the pancreatic branch of the vagus nerve (5). Upper trace of Fig. 1 shows another example of the effect of sweet taste stimulation (5% glucose for 2 min) on the efferent activity of the pancreatic branch of the vagus nerve. As shown in the trace, an application of glucose caused an increase in efferent activity which lasted about 20 min. This observation indicates that even shorter sweet taste stimulation than 5 min is still effective to increase activity of the pancreatic vagus nerve. Lower trace of Fig. 1 presents one example of the effects of taste stimulation with 10% sucrose and 5% NaCl solutions on the efferent activity of the hepatic branch of the vagus nerve. It was observed that an administration of 10% sucrose solution caused an increase, and that of 5% NaCl resulted in a decrease in discharge rate (N = 3). Even taste stimulation with 5% NaCl solution preceded to that with 10% sucrose solution, a suppression in efferent activity was also observed. Similar effects of taste stimulations with 10% sucrose and 5% NaCl solution on efferent activity of the pancreatic branch of the vagus nerve were already reported (6). In contrast to the facilitative effect of sweet taste stimulation on the activity of the pancreatic and hepatic vagus nerve, inhibitory effects were recognized on the efferent activity in the adrenal branch (Fig. 2, panels 1 and 2), pancreatic branch (Fig. 2, panel 2) and hepatic branch (Fig. 2, panel 3) of the splanchnic nerve, following sweet taste stimulation with 5% glucose or 10% sucrose for 5 min. It was further observed that applications of strong salty taste stimulation with 5% NaCl for 5 min resulted in activations of efferent discharges in the adrenal branch (Fig. 2, panel 1, lower trace), pancreatic branch (Fig. 2, panel 2) and hepatic branch (Fig. 2, panel 3) of the splanchnic nerve. Trace 4 in Fig. 2 shows the effects of taste stimulations with 5% glucose, 10% sucrose and 5% NaCl on the efferent activity of the sympathetic nerves innervating interscapular brown adipose tissue. As shown in the trace, opposite to the responses observed on the activity of the adrenal, pancreatic and hepatic branch of the splanchnic (sympathetic) nerve, sweet taste stimulation activated, and strong salty taste stimulation inhibited efferent nerve activity.

3 n

4

10% Sucrose -

5% NaCl -

5% Glucose taa1’ 0’

FIG. 2. Effects of taste stimulation on the efferent activity of adrenal l), pancreatic 2) and hepatic 3) branch of the splanchnic nerve, and that of sympathetic branch innervating interscapular brown adipose tissue 4) in the rat. Vertical bars, 100 impulses per 5 s. Horizontal bars, 10 min.

Table 1 summarizes the effect of sweet and salty taste stimulations on the activity of autonomic nerves innervating visceral organs and brown adipose tissue. In general, it shows the tendency that sweet taste stimulation activates and strong salty taste stimulation inhibits visceral vagal nerve activity, and that splanchnic nerves responded in an opposite manner except responses in the sympathetic nerve innervating brown adipose tissue. DISCUSSION It can be assumed from the experimental

results that the stim-

TABLE 1 EFFECTS OF TASTE STIMULATION ON THE EFFERENT ACTIVITIES THE AUTONOMIC NERVES

10% Sucrose 5% Glucose Vagal pancreatic efferents Vagal hepatic efferents Splanchnic pancreatic efferents Splanchnic hepatic efferents Adrenal sympathetic efferents Sympathetic efferents to IBAT t , facilitation; J , suppression

OF

5% NaCl

TASTE AND EFFERENT AUTONOMIC

167

NERVES

ulation of sweet taste receptors causes an increase in the rate of insulin secretion from the pancreas through the activation of vagal-pancreatic efferents. The preabsorptive increase in insulin level due to taste stimulation reported by Louis-Sylvestre (3) and Steffens (12) can be explained in this light. Shimazu et al. (9-11) reported that electrical stimulation of the vagus nerve enhanced glycogen synthesis in the liver. Their reports support the assumption that the activation of vagal hepatic efferent activity due to sweet taste stimulation may result in an increase in glycogen synthesis in the liver. The reflex increase in vagal pancreatic activity may also contribute to the cephalic exocrine secretion of the pancreas (4,7). The decrease in activities of the adrenal, pancreatic and hepatic branch of the splanchnic nerve due to sweet taste stimulation may cause the reduction in release of catecholamines from the adrenal medulla, noradrenaline from the sympathetic nerve terminals in the pancreas and liver, which in turn cause the decrease in glycogenolysis in the liver and the reduction of glucagon secretion from A cells in the islets of Langerhans. The increase in insulin secretion from B cells can be expected because of the diminution in the liberation of the inhibitory substance (noradrenaline) for insulin secretion (1) from the sympathetic nerve terminals as a result in suppression of efferent activity in the pancreatic branch of the splanchnic nerve. In general, sweet taste stimulation plays a role for the homeostasis of blood glucose through an anticipatory reflex response.

The experimental results further indicated that the strong salty taste stimulation caused opposite responses to those of sweet taste stimulation. For example, increase in splanchnic nerve activity such as activation of adrenal, pancreatic and hepatic efferents, and suppression of vagal pancreatic and hepatic nerve activities. It is likely that these are responses due to stressful stimulation. Brown adipose tissue has been recognized as a major site of energy expenditure through nonshivering thermogenesis. It has also been reported that electrical stimulation of the sympathetic nerves innervating brown adipose tissue resulted in heat production (2). The present study indicated that sweet taste stimulation with 5% glucose and 10% sucrose facilitated efferent activity which in turn may increase heat production from the brown adipose tissue. This response can be explained as a part of diet-induced thermogenesis (8) which is elicited by the oral phase of food intake as an anticipatory response in control of energy balance. The suppression in nerve activity due to strong salty stimulation might be response for stressful stimulation. In conclusion, it is suggested that gustatory signals control visceral functions through autonomic reflex system.

ACKNOWLEDGEMENT

This work was supported sociation of Japan.

by a grant from Umami Manufacturers

As-

REFERENCES Bloom, S. R.; Edwards, A. V. The release of pancreatic glucagon and inhibition of insulin in response to stimulation of the sympathetic innervation. J. Physiol. 253:157-173; 1974. Faim, K. E.; Horwitz, B. A.; Horowitz, J. M. Coupling of signals to brown fat: (Y - and B -adrenergic responses in intact rats. Am. J. Physiol. 232:RlOl-R109; 1977. Louis-Sylvestre, J. Preabsorptive insulin release and hypoglycemia. Am. J. Physiol. 230:50-60; 1976. Naim, M.; Kare, M. R.; Merritt, A. M. Effects of oral stimulation on the cephalic phase of pancreatic exocrine secretion in dogs. Physiol. Behav. 20:563-570; 1978. Niijima, A. Control of liver function and neuroendocrine regulation of blood glucose levels. In: Brooks, C. McC.; Koizumi, K.; Sato, A., eds. Integrative functions of the autonomic nervous system. Tokyo: University of Tokyo Press; 1979:68-83. Niijima, A. Effects of taste stimulation on the efferent activity of the

pancreatic vagus nerve in the rat. Brain Res. Bull. 26:161-164; 1991. 7. Ohara, I.; Otsuka, S.; Yasui, Y. Cephalic phase response of pancreatic exocrine secretion in conscious dog. Am. J. Physiol. 254:G424G428; 1988. 8. Rotwell, N. J.; Stock, M. J. A role for brown adipose tissue in dietinduced thermogenesis. Nature 281:31-35; 1979. 9. Shimazu, T. Glycogen synthesis activity in lever. Regulation by autonomic nerves. Science 156:1256-1257; 1967. 10. Shimazu, T. Regulation of glycogen metabolism in lever by the autonomic nervous system. 5. Activation of glycogen synthetase by vagal stimulation. Biochim. Biophys. Acta 252:28-38; 1971. 11. Shimazu, T.; Fujimoto, T. Regulation of glycogen metabolism in liver by the autonomic nervous system. 4. Neural control of glycogen biosynthesis. Biochim. Biophys. Acta 252:18-27; 1971. 12. Steffens, A. B. Influence of the oral cavity on insulin release in the rat. Am. J. Physiol. 230:1411-1415; 1976.

Effects of taste stimulation on the efferent activity of the autonomic nerves in the rat.

Effects of taste stimulation on the efferent discharges in the pancreatic and hepatic branch of the vagus nerve, and those in the adrenal, pancreatic ...
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