Similar feeding patterns are induced by perifornical neuropeptide Y injection and by food deprivation

doi:10.1016/S0006-8993(97)01289-4

Brain Research

Volume 782, Issues 1–2, 26 January 1998, Pages 271-280

https://doi.org/10.1016/S0006-8993(97)01289-4 Get rights and content

Abstract

Although hypothalamic injections of neuropeptide Y (NPY) induce robust feeding, there is little information about the patterns of feeding elicited by this peptide. To reveal these patterns, NPY (0, 8, 24, 78, 235 pmol/10 nl) was injected into the perifornical hypothalamus (PFH) of satiated adult male rats and their subsequent food intake was monitored every minute for 24 h. For comparison, feeding patterns were similarly observed following fasts of 0, 3, 6, 9, 12, and 24 h. The results demonstrated that NPY and food deprivation both produced dose- or deprivation-dependent increases in food intake that were most evident in the first 6 h. The increased intakes induced by NPY were characterized by combinations of increased meal size and frequency, with the predominant effects being increases in the size of and decreased latency to eat the first meal. Similarly, fasting progressively increased food intake by combinations of increased meal size and frequency, with the predominant effects being increases in the size of and decreased latency to eat the first meal. These similarities between NPY-induced and food deprivation-induced feeding are consistent with a stimulatory role for endogenous NPY in deprivation-induced feeding. These findings also suggest that NPY may increase eating by acting on mechanisms of both meal initiation and of meal termination.

Introduction

Food is usually consumed in discrete meals that vary in size and frequency in patterns characteristic of particular physiological and environmental conditions. Manipulations that enhance food intake increase either meal size or meal frequency 6, 17and the regulation of these parameters may be partially independent [32]. The neural systems regulating meal size and frequency may be distinct neurochemically and anatomically because intracranial injection of some feeding-stimulatory neurotransmitters preferentially increase meal size, while others preferentially increase meal frequency [36]. Thus, analysis of the meal patterns produced by central injection of a neurotransmitter may provide insights about which aspects of eating are regulated by the neurons which employ that neurotransmitter.

Neuropeptide Y (NPY), a neurochemical abundant within many neurons originating or terminating in the hypothalamus [14], has been implicated in the regulation of eating behavior and body weight. Intracranial injection of this phylogenetically conserved peptide induces eating across a wide range of vertebrates, in neonatal as well as adult rats, and throughout the circadian cycle [52]. Endogenous NPY may contribute to feeding because manipulations that suppress endogenous NPY suppress spontaneous feeding 1, 37, 50, 60, and manipulations that increase food intake, such as food deprivation, may elevate NPY release, tissue content and synthesis, and gene expression 4, 28, 47, 67. Although these studies suggest that endogenous NPY may regulate feeding behavior, there is limited data on the patterns of eating elicited by this peptide 27, 35, 38, 39, 58.

Previous meal pattern analyses have shown that low doses of NPY injected into the paraventricular hypothalamus (PVN) elicits the consumption of a single meal 35, 58and that continuous intracerebroventricular (i.c.v.) injection produces consumption of discrete meals at low doses, but induces persistent nibbling at high doses [27]. Since i.c.v. injection of NPY produces a variety of physiological effects [25]that may alter feeding patterns, we chose to characterize the feeding patterns induced by NPY microinjected into the perifornical hypothalamus (PFH), the most sensitive known site for NPY-induced feeding [61]. The major questions were: Is the feeding elicited by PFH injection of NPY organized into discrete meals and, if so, are both meal size and meal frequency increased? Further, since similarities in the feeding patterns induced by NPY and natural conditions may suggest shared neural substrates, we also examined feeding patterns induced by food deprivation, to determine the extent to which they were comparable. Portions of these finding have previously been presented in preliminary form 62, 63.

Section snippets

Subjects and surgery

Twenty adult, Sprague–Dawley, male rats (Simonsen Laboratories, Gilroy, CA), weighing 350–400 g at the start of the experiment, were used. Ten were stereotaxically implanted with an unilateral, 26-gauge, stainless-steel, guide cannula while under Metofane anesthesia. The guide cannula was positioned 1.0 mm dorsal to the PFH. With the incisor bar at −3.3 mm, the stereotaxic coordinates were 7.2 mm anterior to the interaural line, 1.0 mm lateral to the midsagittal sinus, and 7.7 mm ventral to the

Histology

The injection sites (not shown) were centered in the PFH just ventromedial to the fornix at the coronal level of the posterior border of the PVN, an area shown to be maximally sensitive to the feeding-stimulatory effect of NPY [61].

NPY-induced meal patterns

As shown in Fig. 1A, NPY injections produced dose-dependent increases in food intake of up to 230% during the light-phase (F_4,36=48.4, p<0.001). These increases were compensated by complementary dose-dependent decreases in food intake during the subsequent dark-phase

Feeding patterns induced by PFH injection of NPY

These observations demonstrate that, across a wide range of doses, the feeding elicited in rats by acute PFH injection of NPY occurs in discrete meals that are clearly separated by periods without eating. This complements earlier findings that acute PVN injection of a low dose of NPY induces the consumption of a single large meal [58], and that continuous i.c.v. injection of low NPY doses elicited consumption of several meals, whereas, higher doses induced persistent nibbling [27]. That

Acknowledgements

We thank Jack B. Calderone for statistical and graphical consultation. Supported by NIH grant NS 24268.

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Research reportSimilar feeding patterns are induced by perifornical neuropeptide Y injection and by food deprivation

Abstract

Introduction

Section snippets

Subjects and surgery

Histology

NPY-induced meal patterns

Feeding patterns induced by PFH injection of NPY

Acknowledgements

Mol. Brain Res.

Physiol. Behav.

Physiol. Behav.

Physiol. Behav.

Physiol. Behav.

Peptides

Neuroscience

Peptides

Physiol. Behav.

Appetite

Metabolism

Brain Res.

Brain Res. Bull.

Peptides

Physiol. Behav.

Physiol. Behav.

Eur. J. Pharmacol.

Neurosci. Biobehav. Rev.

Pharmacol. Biochem. Behav.

Peptides

Brain Res.

Life Sci.

Brain Res.

Peptides

J. Nutr.

Peptides

Brain Res.

Physiol. Behav.

Physiol. Behav.

Peptides

Brain Res.

Life Sci.

Peptides

Physiol. Behav.

Research report
Similar feeding patterns are induced by perifornical neuropeptide Y injection and by food deprivation