Elsevier

Behavioural Brain Research

Volume 278, 1 February 2015, Pages 520-526
Behavioural Brain Research

Research report
Neuropeptide-Y modulates eating patterns and masticatory muscle activity in rats

https://doi.org/10.1016/j.bbr.2014.10.031Get rights and content

Highlights

  • We investigated how neuropeptide Y (NPY) injection into the lateral ventricle modulates masticatory movements and eating behavior.

  • We analyzed the features of feeding patterns and masticatory muscle activities.

  • Injection of 1 μg NPY promoted eating behavior together with an increased feeding rate and powerful jaw-closing muscle activity.

  • Administration of 10 μg NPY lowers jaw-closing muscle activity during biting and mastication with shorter and more frequent feeding bouts compared to 1 μg NPY.

Abstract

Neuropeptide Y (NPY) is a powerful orexigenic peptide secreted by hypothalamic neurons. The present study investigates how NPY injection into the lateral ventricle modulates masticatory movements and eating behavior. Behavioral experiments showed that cumulative food intake over a 4-h period and latency to eating were increased and decreased, respectively, in NPY-injected rats compared to saline-injected control rats. The feeding time for 2 g pellets was shorter in NPY-injected rats and resulted in an increased feeding rate, with more potent effects observed at 1 μg compared to 10 μg NPY. After injection of 10 μg NPY, a greater number of bouts with shorter average bout duration for eating 2 g, compared to 1 μg NPY, were observed. Furthermore, 10 μg NPY injection resulted in prolonged periods of moving and shortened sleep and grooming. Electromyography recordings from the digastric and masseter muscles showed two distinct patterns of bursts corresponding to the gnawing and chewing phases. After the injection of 1 μg NPY, the burst magnitude of masseter muscle during the gnawing phase increased, reflecting strong jaw-closing muscle activity. The relative integrated EMG of masseter muscle in both phases was smaller following injection of 10 μg NPY in comparison with that of 1 μg NPY. The present study indicates that 1 μg NPY administration promotes feeding behavior together with increased feeding rate and powerful jaw-closing muscle activity; whereas 10 μg NPY administration lowers jaw-closing muscle activity during biting and produces mastication with shorter and more frequent feeding bouts than 1 μg NPY.

Introduction

Feeding behavior, which is essential to human and animal life, is regulated by the feeding and satiety centers in the lateral hypothalamic area and ventromedial nucleus of the hypothalamus, respectively [1], [2]. Leptin, which is produced by white adipose tissue [3], was discovered to play a key role in regulating energy intake and expenditure; since then, several orexigenic neuropeptides, such as neuropeptide-Y (NPY), melanin-concentrating hormone (MCH), agouti-related peptide (AgRP), orexins (orexin-A and orexin-B), and ghrelin [4], [5], [6], [7], [8], have been identified. Although recent studies have demonstrated the physiological effects of these peptides on feeding behavior and body weight, there are few reports concerning the manner in which drug-administered animals actually ingest their foods, e.g., how they bite and masticate food.

NPY is a 36 amino acid neuropeptide that is widely distributed in the central and peripheral nervous systems [9]. It is mainly produced in the arcuate nucleus of the hypothalamus, and exerts several physiological effects, such as increasing food intake [10], reducing anxiety [11], and affecting circadian rhythms [12] and blood pressure [13]. Most notably, the administration of NPY into the third cerebroventricle (TCV), lateral ventricle (LV), and hypothalamic paraventricular nucleus (PVN) produces a potent orexigenic effect that increases both food intake and drinking [14], [15], [16]. It has also been reported that injection of NPY into the PVN increases the intake of carbohydrates and fats [17]. Furthermore, partial changes in feeding behavior, such as eating latency and feeding rate, following the injection of NPY into the TCV have been reported [10], [18]. However, it remains to be determined how NPY administration affects the detailed characteristics of eating patterns and peripherally acting masticatory muscle activity.

Previously, we have described the characteristics of eating patterns in orexin-A administrated rats using video analysis and electromyography (EMG) recording methods [19]. Therefore, the present study aims to elucidate the masticatory activities associated with increased food intake in NPY-administered rats by analyzing the features of feeding patterns. Furthermore, we discuss whether the effects of NPY on feeding behavior, including mastication, are associated with orexins.

Section snippets

Animals and surgical treatment

Adult male Wistar rats (n = 22, weighing 280–300 g) were obtained from the Charles River Breeding Laboratories (Kanagawa, Japan). Rats were separately housed in a controlled environment room (23 °C, 60% humidity, 12-h light:12-h dark cycle) and given ad libitum access to food (MF Pellets; Oriental Yeast, Tokyo, Japan) and water. As with our previous paper [19], rats were anesthetized with sodium pentobarbital (Nembutal, 50 mg/kg i.p., Sigma) and placed into a stereotaxic apparatus (SR-5R; Narishige

Effect of neuropeptide Y on food intake, feeding time, feeding rate, and eating latency

Each rat received an ICV injection of NPY or saline on different days. Histology confirmed that the tip of the cannula was successfully positioned within the left side of the lateral ventricle (Fig. 1A). Cumulative food intake during the 4 h period following administration of 0.1, 1, and 10 μg NPY was increased to 1.5, 7.9, and 10.3 times greater than control, respectively (NPY 1 and 10 μg; P < 0.001, vs. control, Fig. 1Ba). Food intake at hourly intervals reached a peak from onset to 1 h in NPY rats

Discussion

All previous reports concerning the effects of NPY injection on feeding characteristics have focused on feeding parameters for defined periods [14], [15]. The administration of NPY into the TCV, LV, and PVN increased food intake, while injection of NPY into the TCV shortened the latency to initial eating, although the concentrations of NPY were not always proportional to changes in feeding parameters in terms of food intake and feeding time [10], [18]. These behavioral findings suggested that

Competing financial interests

The authors declare no competing financial interests.

Acknowledgments

This work was supported by Grants-in-Aid for Scientific Research (B) (21390535 and 25293409 to M.K) and a Grant-in-Aid for Young Scientists (B) (21791988 to T.T.) from the Japan Society for the Promotion of Science. The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.

References (33)

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