Differential regulation of parvocellular neuronal activity in the paraventricular nucleus of the hypothalamus following single vs. repeated episodes of water restriction-induced drinking

Abstract

Acute activation of the hypothalamic-pituitary-adrenal (HPA) axis releases glucocorticoids to maintain homeostasis, whereas prolonged exposure to elevated glucocorticoids has deleterious effects. Due to the potential benefits of limiting stress-induced glucocorticoid secretion, the present study uses drinking in dehydrated rats as a model to delineate mechanisms mobilized to rapidly inhibit HPA activity during stress. Using Fos expression as an indicator of neuronal activation, the effect of a single or repeated episode of dehydration-induced drinking on the activity of magnocellular and parvocellular neurons in the paraventricular nucleus (PVN) of the hypothalamus was examined. Adult male rats underwent a single episode or repeated (six) episodes of water restriction and were sacrificed before or after drinking water in the AM. Plasma osmolality, vasopressin (AVP), adrenocorticotropic hormone (ACTH) and corticosterone were elevated by water restriction and reduced after drinking in both models. Fos expression was elevated in AVP-positive magnocellular PVN neurons and AVP- and corticotropin releasing hormone (CRH)-positive parvocellular PVN neurons after water restriction. Fos expression was reduced in magnocellular AVP neurons after both models of restriction-induced drinking. In contrast, Fos expression did not change in AVP and CRH parvocellular neurons after a single episode of restriction-induced drinking, but was reduced after repeated episodes of restriction-induced drinking. These data indicate that drinking-induced decreases in glucocorticoids in dehydrated rats involve multiple factors including reduction in magnocellular release of vasopressin and reduction in parvocellular neuronal activity. The differential inhibition of PVN parvocellular neurons after repeated rehydration may reflect a conditioned response to repeated stress reduction.

Vasopressin Increases Locomotion through a V1a Receptor in Orexin/Hypocretin Neurons: Implications for Water Homeostasis

“…Osmotic stimuli activate SON neurons (Mason, 1980) and increase c-fos protein expression in AVP and oxytocin neurons in the SON and PVN (Pirnik et al, 2004;Arnhold et al, 2007). These increases in the release of AVP and oxytocin from SON and PVN might be involved in an activation of orexin neurons under dehydration.…”

Dehydration enhances multiple physiological defense mechanisms in a desert lizard, Heloderma suspectum

“…This trend appears to hold true across many species, including mice (Tsuchida et al, 2004;Bekkevold et al, 2013), rats (Sebaai et al, 2002a,b;Arnhold et al, 2007), quail (Cain and Lien, 1985), cattle (Parker et al, 2004;Hogan et al, 2007), and, under some conditions, humans (Hoffman et al, 1994;Maresh et al, 2006). However, most of these species have been domesticated and/or probably do not regularly experience dehydration in the wild and therefore may not have adapted to coping with a dehydrated state.…”

“…In particular, dehydration increases plasma glucocorticoids, the primary steroid hormones involved in the stress response, in mice (Mus musculus; Tsuchida et al, 2004;Bekkevold et al, 2013), rats (Rattus norvegicus; Sebaai et al, 2002a,b;Arnhold et al, 2007), rabbits (Oryctolagus cuniculus; Kallaras et al, 2004), quail (Colinus virginianus; Cain and Lien, 1985), chickens (Gallus gallus domesticus; Klandorf et al, 1984) and cattle (Bos indicus; Parker et al, 2004). In general, elevated glucocorticoids have initial enhancing effects on immunity, but, if prolonged, they have more depressive effects, although response may also depend on stress hormone concentration (Sapolsky et al, 2000).…”

A two-choice sound localization procedure for detecting lateralized tinnitus in animals

“…One potential source of stress is water deprivation, which increases the levels of hormones and proteins (c-Fos) that are associated with stress (Arnhold, Wotus, & Engeland, 2007;Jørgensen, Knigge, Kjaer, & Warberg, 2002). However, most studies have only looked at the initial effects of restricting an animal's water intake (e.g., 1 or 6 days as in the previously cited studies), and a longer-term study found that hormonal levels in rats on water restriction had returned to normal by 8 weeks (Sakellaris & Vernikos-Danellis, 1974).…”