Subdiaphragmatic vagotomy prevents drinking-induced reduction in plasma corticosterone in water-restricted rats

Abstract

Dehydrated rats exhibit a rapid inhibition of the hypothalamic-pituitary-adrenal axis after rehydration. Drinking activates vagal afferents that project to neurons in the nucleus tractus solitarius (NTS). We hypothesized that when dehydrated rats drink, vagal afferents stimulate NTS neurons initiating inhibition of hypothalamic-pituitary-adrenal activity. Experiments assessed NTS activity by measuring Fos expression. Rats were water restricted for 1 or 6 d, limiting access to water to 30 min/d in the morning. Drinking after single or repeated restriction increased Fos, demonstrating increased NTS activity. We next examined the contribution of the vagus by comparing hormonal responses after total subdiaphragmatic vagotomy or sham surgery. Water restriction for 6 d increased plasma arginine vasopressin (AVP), ACTH, and adrenal and plasma corticosterone in both groups. In sham rats, drinking reduced plasma AVP, ACTH, adrenal and plasma corticosterone by 7.5 min. In total subdiaphragmatic vagotomy rats, whereas drinking reduced plasma AVP, ACTH, and adrenal corticosterone, drinking did not reduce plasma corticosterone. To identify the source of vagal activity, hormonal responses to restriction-induced drinking were measured after common hepatic branch vagotomy (HBV). Although pituitary hormonal responses were not affected by HBV, the adrenal and plasma corticosterone responses to water restriction were reduced; in addition, drinking in HBV rats decreased adrenal corticosterone without changing plasma corticosterone. These data indicate that an intact vagus is necessary to reduce plasma corticosterone when water-restricted rats drink and that the common hepatic vagal branch contributes to the response. These findings implicate the vagus in augmenting rapid removal of circulating corticosterone during relief from stress.

Figure 1

Immunolabeling for Fos in rostral and caudal NTS neurons. Representative labeling of neurons in the rostral (A) and caudal (B) NTS in rats that underwent repeated (6 d) water restriction and received water for 30 min on d 6. Black arrowhead indicates Fos-positive neuron. Scale bar, 100 μm. DMV, DMX; imNTS, intermediate NTS; mNTS, medial NTS; ST, solitary tract; vlNTS, ventrolateral NTS.

Figure 2

The effect of a single and repeated episode of water restriction and drinking on the total number of Fos-positive neurons in the NTS. Total number of Fos-positive neurons in the rostral (interaural level −11.8 to −13.3 mm; A and C) and caudal (interaural level −13.6 to −14.8 mm; B and D). The rostral and caudal NTS was further divided into medial (A) and ventrolateral (C) or medial (B) and intermediate (D) according to Paxinos and Watson (24). Values represent means ± sem: n = 6 per group. *, P < 0.05 vs. ad lib; ^, P < 0.05 vs. WR of same cohort.

Figure 3

The effect of TSdV on pituitary-adrenal hormones. Comparison between sham vagotomy and TSdV in plasma vasopressin (A), ACTH (B), adrenal corticosterone (C), and plasma corticosterone (D) from ad lib and WR rats before and 7.5 or 15 min after drinking. Values represent means ± sem number per group as listed for Table 1. *, P < 0.05 vs. ad lib; ^, P < 0.05 vs. WR of same cohort; #, P < 0.05 vs. sham-WR. Compound B, Corticosterone.

Figure 4

The effect of common HBV on pituitary-adrenal hormones. Comparison between sham vagotomy and HBV in plasma vasopressin (A), ACTH (B), adrenal corticosterone (C), and plasma corticosterone (D) from WR rats before and 7.5 after drinking. Values represent means ± sem number per group as listed for Table 2. #, P < 0.05 vs. sham-WR; ^, P < 0.05 vs. WR of same cohort.