Brain Research Bulletin,

Vol. 26, pp. 161-164. 0 Pergamon Press plc, 1991. Printed in the U.S.A

0361-9230/91

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Effects of Taste Stimulation on the Efferent Activity of the Pancreatic Vagus Nerve in the Rat’ AKIRA

Department

of Physiology,

NIIJIMA

Niigata University School of Medicine,

Received

Niigata, 951 Japan

5 July 1990

A. Effecrs of taste stimulation on the efferent activity of the pancreatic vagus nerve in the rat. BRAIN RES BULL 26( 1) 161-164, 1991 .-The effect of taste stimulation on the efferent discharges in the pancreatic branch of the vagus nerve was studied in anesthetized rats. An increase in discharge rate following taste stimulation with 10% sucrose over the tongue for 5 or 3 min, and a decrease of it following an application of 5% NaCl for the same duration were observed in normal as well as in decerebrated rats. It was further observed that local anesthesia of the surface of the tongue blocked the reflex response originated by taste stimulation. The results indicate the existence of gustatory vago-pancreatic reflex which plays an important role for cephalic phase secretion.

NIIJIMA,

Taste stimulus

Pancreatic

vagus nerve

Insulin

Reflex

Cephalic phase

access to food and water before the experiment. Rats were anesthetized intraperitoneally with 700 mg/kg of urethane and 50 mgl kg of chloralose. A trachea cannula was inserted. Nerve filaments were dissected from the pancreatic branch of the vagus nerve which is branched off from the celiac branch of the vagus nerve and runs along the side of splenic artery. Under a dissecting microscope, nerve filaments were isolated from the central cut end of the pancreatic branch to record the efferent nerve activity with a pair of silver wire electrodes. Nerve activity was amplified and displayed on an oscilloscope and stored on magnetic tape. All nervous activity was analysed after conversion of raw data to standard pulses by a window discriminator which separated discharges from background noise. A rate meter with a reset time of 1 or 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. The ECG was monitored throughout the experiment. For the sweet taste stimulation 10% sucrose solution was used. As a control, 5% NaCl solution was used for strong salty taste stimulation. The temperature of solutions was about 26°C. These solutions were applied to the tongue surface with a syringe by holding the tongue outside the buccal cavity. Each trial required 3-5 min to spread the solution continuously over the tongue at a rate of 0.8-l .O ml/min, and the tongue was flushed with distilled water at the end of each taste stimulation. The effect of taste stimulation on the efferent activity was in-

IN 1976 Steffens (7) reported an increase in plasma insulin in rats during the fist minute of a meal. This increase preceded the wellrecognized rise of insulin level, which coincided with the increase in blood glucose. He named this phenomenon the early rise in insulin response (EIR) and indicated that the oral cavity plays a major role in bringing it about. The same type of response was also investigated by Louis-Sylvestm (2). In 1979 Niijima observed the effect of sweet taste stimulation on the efferent activity of the pancreatic vagus nerve. In his preliminary report (4) he described that an application of 10% glucose for 5 min to the tongue caused an increase in the efferent activity of the pancreatic branch of the vagus nerve in anesthetized rat. His observations suggest that stimulation of sweet taste receptors causes an increase in the rate of insulin secretion from the pancreas through the activation of vagal pancreatic efferents as a gustatory reflex, and explains one of the mechanisms of cephalic phase of insulin secretion. This paper mainly deals with the effects of sweet and salty taste stimulation on the activity of the vagal pancreatic efferents in normal and decerebrated rats to examine the mechanism of cephalic phase of insulin secretion. METHOD

Wister rats weighing about 300 g were used. Animals had free

‘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.

161

NIIJIMA

162

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I. Effects of taste stimulations with 10% sucrose and 5% NaCl solutions to the tongue surface on efferent discharge rate of pancreatic branch of the vagus nerve. Top trace, heart rate. Middle trace, time course of nerve activity. Lower traces, (a) nerve activity just before sucrose stimulation; (b) nerve activity 5 min after sucmse stimulation.

vestigated by comparing the mean number of spikes per second over 20 s (i.e., mean value of 20 successive measured samples) just before taste stimulations and 5 min after rinsing. Significance was determined by Student’s t-test. Decerebration was made at the midcollicular level. After making a hole at the occipital part of the skull (posterior to the bregma) a small knife was advanced along the side of the tentorium cerebelli until it reaches the bottom of the skull to make complete decerebration which was confirmed after each experiment.

Before administration of 4% xylocaine, an application of 10% sucrose for 3 min caused a long-lasting (about 30 min) activation of the efferent activity, however, 3 min after administration of 4% xylocaine taste stimulation with 10% sucrose caused no remarkable changes in efferent discharge rate (Fig. 2, upper trace). Twenty minutes after rinsing the tongue with distilled water, taste stimulation by 10% sucrose was given again, which caused similar increase in discharge rate as that observed before xylocaine anesthesia.

RESULTS Figure 1 shows the effect of oral stimulation of 10% sucrose and 5% NaCl on the multiunits efferent activity of the pancreatic branch of the vagus nerve. An increase in discharge rate started about 3 min after onset of taste stimulation by 10% sucrose which lasted approximately 20 min, and the peak was reached about 5 min after the rinsing of the tongue. The rate of discharge at the peak was about 166% of the control value in this particular preparation. On the contrary, an application of 5% NaCl for five min caused a suppression in discharge rate which also lasted about 20 min. The degree of suppression was about 25% of the nerve activity just before NaCl stimulation. No change in heart rate before, during and after taste stimulations by 10% sucrose and 5% NaCl. In contrast to the effects of 10% sucrose and 5% NaCl stimulation, oral stimulations with 0.9% NaCl solution and with distilled water for 5 min were without effect (3 observations each). The effect of temperature on the test solutions and mechanical factors of stimulation procedure on changing in efferent activity can be neglected because there are no differences in temperature of the taste solutions and procedure of each taste stimulation. Figure 2 shows the effects of 10% sucrose stimulation before and after the administration of 4% xylocaine over the tongue.

4 SyoXylocaine 10 96 Sucrose

I 10 ~Sucrose

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10 %Sucrose

3%NaCl

5%NaCI

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GUSTATORY

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.

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PIG. 4. Effects of taste stimulations anesthetized and decerebrated rat.

5% NaCl (N=6)

PIG. 3. Effects of taste stimulation on the discharge vagus nerve. (Values are mean + S.E.M.)

0

rate of pancreatic

In this preparation it was also observed that a strong salty taste stimulation by 5% NaCl solution resulted in a remarkable suppression, and a little weaker stimulation by 3% NaCl solution caused no change in discharge rate (Fig. 2, lower trace). The facilitatory effect of sweet taste stimulation by 10% sucrose solution on efferent discharge rate was observed in eight preparations. The mean efferent discharge rate just before stimulation was 5.2OkO.33 impulses/s (meancS.E.), and that at 5 min after onset of stimulation was 7.5 1 t 0.56 impulses/s. A significant increase in discharge rate was recognized (n=8, pcO.02). The suppressive effect of 5% NaCl stimulation was studied on six preparations. Just before the NaCl stimulation, the mean discharge rate was 6.03 20.24 impulses/s (mean?S.E.). The mean discharge rate at 5 min after onset of NaCl stimulation was 4.0 2 0.53 impulses/s. The difference was significant (n = 6, pcO.02) (Fig. 3). Figure 4 shows the effects of taste stimulation on an anesthetized and decerebrated rat. Taste stimulations were applied during the period of stable firings of efferent discharges after 30 min of control recordings which started 30-60 min after decerebration procedure. As shown in the figure 10% sucrose administration for 5 min caused an increase in discharge rate which lasted about 25 min, and a suppression in discharge rate with duration of 20 min was originated in response to 5% NaCl stimulation for five minutes. The experiment was further conducted on another decerebrated rat. It was recognized that the type of responses was basically similar to that of normal anesthetized rat. DISCUSSION

The experimental results indicate that sweet taste stimulation by 10% sucrose solution accelerates, and strong salty taste stim-

-10min

with 10% sucrose and 5% NaCl in

ulation by 5% NaCl solution suppresses efferent activity of the pancreatic vagus nerve, and the response is blocked by local anesthesia of the tongue, suggesting gustatory vago-pancreatic reflex. The prompt increase in plasma insulin level following food ingestion in the rat reported by Steffens (7) can be explained in this light. The suppression in efferent activity by strong salty taste stimulation seems to be an inhibitory response of the vagus nerve due to the stressful stimulation. Steffens (6) reported that during a meal insulin increases already in the first minute and, if carbohydrate is present in the food, the blood glucose level starts to rise in the third minute which causes a second increase in insulin. He further described that the second increase in insulin level seems to coincide with the increase in blood glucose level. The differences between quick insulin rise during a meal and a slow increase in efferent activity of the pancreatic vagus due to a sweet taste stimulation in anesthetized rat might be explained in the following way. In the conscious rat insulin secretion during food intake is an active response which includes activation of the higher center, however, in anesthetized rat the response due to sweet taste stimulation is a passive reflex phenomenon without activation of the cortex and other higher centers. Probably, differences between these experimental conditions resulted in different time courses of the response. There is a possibility that the reflex activation of vago-pancreatic nerve by sweet taste stimulation also contributes to the cephalic phase response of pancreatic exocrine secretion. It has been reported by several workers that a remarkable response in pancreatic exocrine secretion in cephalic phase is obtained by palatable taste stimuli such as sucrose (1, 3, 5). It can be assumed that gustatory vago-pancreatic reflex plays an important role in anticipatory responses on endocrine secretion of the pancreas as well as exocrine secretion of the digestive organs. Observations on the decerebrated rats suggest the existence of the center of gustatory vago-pancreatic reflex in the brainstem, although the hypothalamus may play some role in modulation on the activity of the reflex center.

REFERENCES 1. Behrman, H. R.; Kare, M. R. Canine pancreatic secretion in response to acceptable and aversive taste stimuli. hoc. Sot. Exp. Biol. Med. 129:343-346; 1968. 2. Louis-Sylvestre, J. Preabsorptive insulin release and hypoglycemia. Am. J. Physiol. 2305060; 1976. 3. 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. 4. 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.

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5. Ohara, I.; Otsuka, S.; Yasui, Y. Cephalic phase response of pancreatic exocrine secretion in conscious dog. Am. J. Physiol. 254:G424G428; 1988. 6. Steffens, A. B. Rapid absorption of glucose in the intestinal tract of

NIIJIMA

the rat after ingestion of a meal. Physiol. Behav. 4:829-832; 1969. 7. 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 pancreatic vagus nerve in the rat.

The effect of taste stimulation on the efferent discharges in the pancreatic branch of the vagus nerve was studied in anesthetized rats. An increase i...
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