Elsevier

Neuropeptides

Volume 69, June 2018, Pages 9-18
Neuropeptides

Appetite-associated responses to central neuropeptide Y injection in quail

https://doi.org/10.1016/j.npep.2018.03.001Get rights and content

Highlights

  • Quail desensitize to central neuropeptide Y injection at a considerably lower threshold than other species.

  • Increased food intake after neuropeptide Y was coupled to an increase in c-Fos immunoreactivity and NPYR2 mRNA abundance in the arcuate nucleus.

  • Behavioral changes after central neuropeptide Y injection are indicative of a shift towards feeding behavior.

Abstract

The appetite-associated effects of neuropeptide Y (NPY) have been extensively studied in mammalian models. Less knowledge exists for other vertebrate species including birds. The aim of this study was to determine the effects of central injection of NPY on feeding behavior and hypothalamic physiology in 7 day-old Japanese quail (Coturnix japonica). During the light cycle, intracerebroventricular injection of 1.9 pmol, 0.5, and 1.0 nmol doses of NPY did not affect food intake, 0.031 to 0.13 nmol increased food intake, and 2.0 nmol NPY decreased food intake, in comparison to vehicle injection. Multiple doses of NPY stimulated water intake, but when food was not available, water intake was not affected. When injected during the dark cycle, NPY did not influence food intake. NPY-injected chicks had more c-Fos immunoreactive cells in the arcuate nucleus of the hypothalamus (ARC) and greater hypothalamic agouti-related peptide and neuropeptide Y receptors 1 and 2 (NPYR1 and NPYR2, respectively) mRNA than vehicle-injected chicks. Within the ventromedial hypothalamus, NPY-treated chicks expressed less NPYR1 mRNA, within the dorsomedial hypothalamus less NPY mRNA, and in the ARC greater NPYR2 mRNA than vehicle-injected chicks. Lastly, quail injected with NPY increased feeding pecks, escape attempts, and time spent preening, while locomotion, the number of steps, and time spent perching decreased compared to chicks injected with the vehicle. Results demonstrate that NPY stimulates food intake in quail, consistent with mammals and other avian species, but with some unique responses at the molecular level that are not documented in other species.

Introduction

Since its discovery over three decades ago (Tatemoto, 1982), neuropeptide Y (NPY), a potent orexigenic factor and one of the most abundant and ubiquitously-expressed neuropeptides in both the central and peripheral nervous systems (Chronwall and Zukowska, 2004), has been implicated in a wide range of physiological responses including locomotion (Heilig et al., 1989), memory (Flood and Morley, 1989), anxiety (Giesbrecht et al., 2010; Reichmann and Holzer, 2016), epilepsy (Klapstein and Colmers, 1997), circadian rhythm (Sindelar et al., 2005), reproduction (Sirotkin et al., 2015), adipose tissue biology (Zhang et al., 2014, 2015) and cardiovascular function (Jacques and Abdel-Samad, 2007; Zhu et al., 2016). The most well studied function of NPY is food intake regulation. Central injection of NPY increases food intake in a range of vertebrates including rats (Clark et al., 1984; Levine and Morley, 1984; Morley et al., 1987b), sheep (Miner et al., 1989), pigs (Parrott et al., 1986), white-crowned sparrows (Richardson et al., 1995), and chickens (Kuenzel et al., 1987; Newmyer et al., 2013). Repeated administration of NPY was associated with hyperphagia and increased body weight gain leading to obesity in rats (Beck et al., 1992; Dryden et al., 1995).

A major brain center mediating homeostatic food intake is the hypothalamus, where the main source of NPY is the arcuate nucleus (ARC; also known as the infundibular nucleus in birds) where it is co-expressed with another orexigenic factor, agouti-related peptide (AgRP) (Broberger et al., 1998). The ARC NPY neurons have projections to other hypothalamic regions associated with food intake (Chronwall et al., 1985). In mammals, the hunger-stimulating effect of NPY is mainly mediated via receptor sub-types 1 and 5 (NPYR1 and R5, respectively) (Mercer et al., 2011). The ARC also contains satiety function-associated neurons that co-express proopiomelanocortin (POMC) and cocaine- and amphetamine regulated transcript (CART) (Mercer et al., 2011). These neurons also express NPY receptors (Ghamari-Langroudi et al., 2005), signaling through which is associated with reduced anorexigenic tone in mammals (Mercer et al., 2011). Furthermore, 24 hour fasted Japanese quail exhibited a 1.5 fold increase in NPY mRNA expression (Boswell et al., 2002) and a 2.2 fold increase in AgRP mRNA expression (Phillips-Singh et al., 2003). Less is known about the hypothalamic mechanisms underlying the appetite-associated function of NPY in birds. In chickens, central NPY injection is associated with activation of the paraventricular nucleus (PVN) and lateral hypothalamic area (LHA) (Newmyer et al., 2013), and co-injection with alpha-melanocyte stimulating hormone (α-MSH, a derivative of POMC) leads to a reduction in food intake (Cline and Smith, 2007). Moreover, relative quantities of hypothalamic NPYR1 and melanocortin receptor 4 (MC4R) mRNA were reduced by NPY in chicks that consumed a high protein and high carbohydrate diets, respectively (McConn et al., 2017).

Most feeding behavior research in birds utilizes the domestic chicken, Gallus gallus. Of all avians, the chicken has undergone the most intense artificial selection for specific traits, which has likely led to correlated responses in the neurobiology associated with food intake. The Japanese quail (Coturnix japonica) has undergone less intense selection than the chicken but still adapts well to laboratory cage environments and handling. The objective of this research was to determine the effects of centrally-injected NPY on feeding behavior and hypothalamic physiology in Japanese quail.

Section snippets

Animals

Japanese quail were bred and hatched in our vivarium. The breeder flock was established with eggs donated by Dr. Mike Lacy at the University of Georgia. Upon removal from the hatcher, chicks were group caged in a brooder for 4 days, then individually in galvanized wire cages (8 cm wide, 7 cm deep and 8 cm high) in a room at a constant temperature of 35 ± 1 °C, 50 ± 5% relative humidity, with a 14-h light/10-h dark period (lights on at 05:00 h). At all times, unless otherwise noted, chicks had ad

Food and water intake: 0.5, 1, and 2 nmol NPY

At the highest dose evaluated, NPY decreased food intake (Fig. 1). On a cumulative basis (Fig. 1A) chicks injected with 2.0 nmol NPY decreased food intake, but only at 30 min post-injection. At 60 min post-injection, there was increased food intake in 1.0 nmol NPY-injected chicks. Food intake was not different in treated vs. vehicle-injected chicks at any other time or dose, although at 180 min, intake was greater in 1 than 0.5 nmol-injected chicks. On a non-cumulative basis (Fig. 1B), chicks

Discussion

The present findings demonstrate that NPY increased food intake in quail, consistent with effects reported for chickens, however magnitude differences were detected between age groups and among broiler (meat-type) and layer (egg-laying-type) chickens. For example, in day-old broilers, food intake doubled after central injection of 1.2 and 2.1 nmol NPY 60 min post injection (Kuenzel et al., 1987), whereas intake increased fivefold over controls in response to 2.1 nmol NPY in 4 week-old broilers (

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