Association between the amygdala and nucleus of the solitary tract in μ-opioid induced feeding in the rat

doi:10.1016/S0006-8993(98)00602-7

Brain Research

Volume 802, Issues 1–2, 17 September 1998, Pages 184-188

https://doi.org/10.1016/S0006-8993(98)00602-7 Get rights and content

Abstract

The central nucleus of the amygdala (CNA) and the nucleus of the solitary tract (NTS) are important in the regulation of ingestive behavior. We evaluated whether opioid–opioid signaling between the CNA and rostral NTS (rNTS) affect feeding behavior. To test this, rats were doubly cannulated with one cannula placed in the rNTS and one cannula in the CNA, allowing for co-administration of an opioid agonist into one site and an opioid antagonist into the other. Tyr-D-Ala-Gly-(me) Phe-Gly-ol (DAMGO) (2 nmol) injected into the CNA (CNA DAMGO) increased feeding more than two-fold compared to the vehicle-injected rats. This increase in food intake was blocked when doses of 26.5 and 79 nmol of naltrexone (NTX) were injected into the rNTS. In the reverse situation, rNTS DAMGO increased food intake above control levels, and CNA NTX blocked DAMGO-induced feeding when administrated in doses of 26.5 and 79 nmol. This suggests that a bi-directional opioid–opioid signaling pathway exists between the CNA and the rNTS which influences feeding via μ-opioid receptors.

Introduction

The central nucleus of the amygdala (CNA) and the nucleus of the solitary tract (NTS) are important in many autonomic functions including regulation of ingestive behavior. Lesions of, or opioid agonist administration into either of these brain nuclei result in increased food intake 3, 6, 9, 10, 13, 15, 18, 30, 31. The μ-agonist DAMGO is a potent opioid ligand that increases feeding in both of these brain nuclei 6, 15. Co-administration of naloxone, an opioid antagonist, along with DAMGO into the CNA blocks DAMGO-induced increase in food intake [6]. The effect of this drug combination on food intake has not been evaluated in the NTS. However, central as well as intra-NTS injection of naloxone decreases deprivation-induced feeding and neuropeptide Y (NPY)-induced feeding 14, 16, 19.

There is anatomical evidence that the CNA receives afferent projections from the NTS and that the NTS receives efferent projections from the CNA 11, 21, 28. Petrov et al. [24]reported that electrical stimulation of the CNA induced Fos-like immunoreactivity in the NTS and various hypothalamic nuclei suggesting a neural connection between the CNA and the NTS. It has been suggested that the amygdaloid complex may modulate activity of midbrain and caudal brainstem centers via the hypothalamus 22, 24, 25, 26. In addition to such direct data demonstrating connectivity between the CNA and NTS, other studies have shown that these two nuclei are involved in various physiological events. Ritter and Dinh [29]reported that 2-deoxy-glucose and 2-mercaptoacetate induced Fos-like immunoreactivity in both nuclei, suggesting participation in the metabolic control of feeding. Others have shown that doses of 2,5-anhydro-d-mannitol that reliably stimulate food intake induced Fos-like immunoreactivity in both nuclei as well as other sites [12]. Several reports have also indicated neuronal connection between the CNA and the NTS involving GABAergic neurons as well as μ-opioid receptors in both nuclei 1, 2, 27, 32.

Based on the above data, we evaluated whether an opioid–opioid signaling pathway exists between the CNA and rNTS which affects feeding behavior. To study this interaction, we stimulated feeding by injecting DAMGO into one of these two nuclei and attempted to block feeding by simultaneously injecting the opioid antagonist naltrexone (NTX) into the other site.

Section snippets

Materials and methods

Male Sprague–Dawley rats (Harlan, Madison, WI), weighing 225–250 g, were individually housed in conventional hanging cages with a 12 h light/12 h dark photoperiod (lights on at 0700) in a temperature controlled room (21–22°C). Rats were anesthetized with Nembutal (40 mg/kg) and fitted with 26 gauge stainless steel guide cannula (Plastics One, Austin, TX) in the CNA and/or in the rostral region of the NTS (at the level of the rostral extent of the nucleus ambiguus) (rNTS). Stereotaxic

Results

NTX given 15 min prior administration of DAMGO into the rNTS significantly blocked DAMGO-induced food intake (F_2,26=7.82, p=0.004). The 26.5 nmol dose of NTX inhibited DAMGO-induced feeding by approximately 45% compared to the group receiving DAMGO/saline (Fig. 2).

In the second experiment, we found a main effect of drug administration on food intake (F_5,65=9.802, p=0.0001). CNA DAMGO increased feeding more than two fold compared to the vehicle-injected rats (p=0.0001) (Fig. 3). When doses of

Discussion

In the present study, we evaluated potential opioid–opioid signaling between two brain sites known to be involved in the regulation of feeding, the rNTS and the CNA. It is known that injection of opioid ligands into either one of these sites increases feeding behavior 7, 8, 15, 16, 17, 18, 20. Blockade of opioid receptors in these sites decreases food intake stimulated by opioids or by food deprivation 6, 15, 16, 19, 31.

As noted by others, we found that DAMGO, a ligand selective for the

Acknowledgements

This research was supported by the General Research Funds of the Veterans Administration Medical Center, the National Institute of Diabetes and Digestive and Kidney Diseases Grant DK 50456 and by the National Institute of Drug Abuse Grant DA-03999. We thank Jim Pomonis and Martha Grace for their technical assistance.

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Research reportAssociation between the amygdala and nucleus of the solitary tract in μ-opioid induced feeding in the rat

Abstract

Introduction

Section snippets

Materials and methods

Results

Discussion

Acknowledgements

Brain Res.

Brain Res.

Neuropharmacology

Life Sciences

Brain Research

Brain Res.

Physiol. Behav.

Neuroscience

Peptides

Pharmacol. Biochem. Behav.

Peptides

Neuroscience

J. Chem. Neuroanat.

Brain Res.

Brain Res.

Brain Res.

Research report
Association between the amygdala and nucleus of the solitary tract in μ-opioid induced feeding in the rat