Vago-sympathoadrenal reflex in thermogenesis induced by osmotic stimulation of the intestines in the rat - PubMed (original) (raw)

Vago-sympathoadrenal reflex in thermogenesis induced by osmotic stimulation of the intestines in the rat

Toshimasa Osaka et al. J Physiol. 2002.

Abstract

Duodenal infusion of hypertonic solutions elicits osmolality-dependent thermogenesis in urethane-anaesthetized rats. Here we investigated the involvement of the autonomic nervous system, adrenal medulla and brain in the mechanism of this thermogenesis. Bilateral subdiaphragmatic vagotomy greatly attenuated the first hour, but not the later phase, of the thermogenesis induced by 3.6 % NaCl (10 ml kg(-1)). Neither atropine pretreatment (10 mg kg(-1), I.P.) nor capsaicin desensitization had any effect on the osmotically induced thermogenesis, suggesting the involvement of non-nociceptive vagal afferents. Bilateral splanchnic denervation caudal to the suprarenal ganglia also had no effect, suggesting a lack of involvement of spinal afferents and sympathetic efferents to the major upper abdominal organs. Adrenal demedullation greatly attenuated the initial phase, but not the later phase, of thermogenesis. Pretreatment with the beta-blocker propranolol (20 mg kg(-1), I.P.) attenuated the thermogenesis throughout the 3 h observation period. The plasma adrenaline concentration increased significantly 20 min after osmotic stimulation but returned to the basal level after 60 min. The plasma noradrenaline concentration increased 20 min after osmotic stimulation and remained significantly elevated for 120 min. Therefore, adrenaline largely mediated the initial phase of thermogenesis, and noradrenaline was involved in the entire thermogenic response. Moreover, neither decerebration nor pretreatment with the antipyretic indomethacin (10 mg kg(-1), S.C.) had any effect. Accordingly, this thermogenesis did not require the forebrain and was different from that associated with fever. These results show the critical involvement of the vagal afferents, hindbrain and sympathoadrenal system in the thermogenesis induced by osmotic stimulation of the intestines.

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Figures

Figure 1

Figure 1. Effects of denervation of vagus or splanchnic nerves, pretreatment with atropine, or capsaicin desensitization on responses to duodenal infusion of hypertonic NaCl

Metabolic rate (A) and _T_c (B) following vagotomy (•, n = 4), splanchnic denervation (▾, n = 4), atropine pretreatment (○, n = 4) and capsaicin desensitization (▿, n = 4). Hypertonic (3.6 %) NaCl was infused into the duodenum at a volume of 10 ml kg−1 for 10 min. The horizontal bar shows the period of NaCl infusion. The metabolic rate of vagotomized rats was significantly lower than other rats at 25–30 min, and the energy expenditure during the first hour was significantly lower in vagotomized rats than in the other groups, although energy expenditure during the 1–3 h period was comparable among all groups. Values are means and vertical bars show

s.e.m.

Figure 2

Figure 2. Effects of adrenal demedullation on duodenal hypertonic NaCl-induced responses

The metabolic rate (A), _T_c (B), and heart rate (C)of adrenal-demedullated rats (•, n = 6) and sham-operated control rats (○, n = 5). The metabolic rate of adrenal-medullated rats was significantly lower than that of sham-operated control rats for 20–50 min following infusion of 3.6 % NaCl, and the initial energy expenditure during the first hour in adrenal-demedullated rats was significantly lower than in control rats, although energy expenditure during the 1–3 h period was comparable. The horizontal bar shows the period of NaCl infusion.

Figure 3

Figure 3. Contribution of β-adrenoceptors to the osmotically induced thermogenesis

The effect on metabolic rate (A), _T_c (B) and heart rate (C) of duodenal infusion of 3.6 % NaCl in propranolol-treated (•, n = 5) and control (▵, n = 5) rats, and 0.9 % NaCl infusion in propranolol-treated rats (○, n = 5). The propranolol-treated rats exhibited a significantly smaller thermogenic response than the control rats. However, propranolol-treated rats expended energy to a significantly higher degree after the 3.6 % NaCl infusion than after the 0.9 % NaCl infusion. Reflecting the changes in metabolic rate, _T_c decreased in propanolol-treated rats after infusion of 0.9 % NaCl, but not after infusion of 3.6 % NaCl, and increased in control rats that had been infused with 3.6 % NaCl without administration of propranolol. Administration of propranolol alone significantly decreased the basal heart rate, and the changes in heart rate were similar between rats infused with 0.9 % NaCl and 3.6 % NaCl. We did not record the heart rate of the control group. The arrows show the time of propranolol administration; the horizontal bar shows the period of NaCl infusion.

Figure 4

Figure 4. Changes in plasma levels of noradrenaline, adrenaline and dopamine after infusion of 3.6 % NaCl, 20 % glucose or 0.9 % NaCl

Changes in plasma levels of noradrenaline (A), adrenaline (B), and dopamine (C) after infusion of 3.6 % NaCl (○, n = 6), 20 % glucose (▾, n = 6) or 0.9 % NaCl (•, n = 5). A, infusion of 3.6 % NaCl or 20 % glucose, but not 0.9 % NaCl, markedly increased the plasma adrenaline level at 20 min, although the level rapidly returned to basal. B, the plasma noradrenaline level increased after the infusion of either hypertonic solution, and the significant increase lasted for 2 h in the rats infused with 3.6 % NaCl, and for 1 h in the rats infused with 20 % glucose. C, the infusion of neither 3.6 % NaCl nor 20 % glucose had any effect on the plasma level of dopamine. * Significant difference from the corresponding value for the group infused with 0.9 % NaCl.

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