Sucrose consumption increases naloxone-induced c-Fos immunoreactivity in limbic forebrain

Graduate Program in Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455, USA.
AJP Regulatory Integrative and Comparative Physiology (Impact Factor: 3.53). 04/2000; 278(3):R712-9.
Source: PubMed

ABSTRACT Opioids have long been known to have an important role in feeding behavior, particularly related to the rewarding aspects of food. Considerable behavioral evidence suggests that sucrose consumption induces endogenous opioid release, affecting feeding behavior as well as other opioid-mediated behaviors, such as analgesia, dependence, and withdrawal. In the present study, rats were given access to a 10% sucrose solution or water for 3 wk, then they were injected with 10 mg/kg naloxone or saline. Brains were subsequently analyzed for c-Fos immunoreactivity (c-Fos-IR) in limbic and autonomic regions in the forebrain and hindbrain. Main effects of sucrose consumption or naloxone injection were seen in several areas, but a significant interaction was seen only in the central nucleus of the amygdala and in the lateral division of the periaqueductal gray. In the central nucleus of the amygdala, naloxone administration to those rats drinking water significantly increased c-Fos-IR, an effect that was significantly enhanced by sucrose consumption, suggesting an upregulation of endogenous opioid tone in this area. The data from this study indicate that the central nucleus of the amygdala has a key role in the integration of gustatory, hedonic, and autonomic signals as they relate to sucrose consumption, if not to food intake regulation in general. Furthermore, the data from this study lend further support to the hypothesis that sucrose consumption induces the release of endogenous opioids.

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    • "Sugar appetite in rodents is mediated in part by brain dopamine (DA) and opioid transmitter systems. Thus, sugars can release brain DA (e.g., Avena et al., 2006; Hajnal and Norgren, 2001; Hajnal et al., 2004; Hernandez and Hoebel, 1988, 1990; Rada et al., 2005) and opioids (e.g., Castro and Berridge, 2014; Colantuoni et al., 2001; Papaleo et al., 2007; Pomonis et al., 2000; Yamamoto et al., 2000). Opioid receptor antagonism with naloxone or naltrexone (NTX) significantly reduces intakes of sucrose (Glass et al., 1996; Kirkham and Cooper, 1988a, 1988b; Levine et al., 1982, 1995; Rockwood and Reid, 1982; Sclafani et al., 1982) and saccharin (Cooper, 1983; Lynch, 1986; Lynch and Libby, 1983) as well as fat (Cooper et al., 1985; Weldon et al., 1996) in rats. "
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    ABSTRACT: Sugar and fat intake in rodents are mediated in part by brain dopamine (DA) and opioid neurotransmitter systems although important strain differences exist. Thus, whereas sucrose intake of BALB/c and SWR mice was reduced by DA D1 (SCH23390: SCH) receptor antagonism, opioid (naltrexone: NTX) receptor antagonism reduced intake only in BALB/c mice. Both SCH and NTX reduced fat (Intralipid) intake in SWR, but not BALB/c mice. The present study extended this pharmacological analysis to caloric and non-caloric sweeteners by examining whether fructose (8%) or saccharin (0.2%) intakes were differentially suppressed in BALB/c and SWR mice by SCH (50–1600 nmol/kg) or NTX (0.01–5 mg/kg) over a 5- to 120-min time course. SCH significantly reduced fructose (200–1600 nmol/kg) and saccharin (50–1600 nmol/kg) intakes in both strains as did NTX (0.1–5 mg/kg). Antagonist ID40 potencies were < 50 nmol/kg for SCH and 0.9 mg/kg for NTX in inhibiting saccharin intake, and 1234 nmol/kg for S CH and 5 mg/kg for NTX in inhibiting fructose intake in BALB/c mice. For SWR mice, the ID40 potencies were < 50 nmol/kg for SCH and 0.02 mg/kg for NTX in inhibiting saccharin intake, and 298 nmol/kg for SCH and 2.6 mg/kg for NTX in inhibiting fructose intake. Thus, saccharin intake was similarly reduced by SCH and NTX in BALB/c and SWR mice, but greater potencies of opioid (1.9-fold) and DA D1 (4-fold) receptor antagonism of fructose intake were observed in SWR relative to BALB/c mice, indicating strong strain differences.
    Pharmacology Biochemistry and Behavior 01/2015; 131. DOI:10.1016/j.pbb.2015.01.010 · 2.82 Impact Factor
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    • "The central nucleus—the main output way station of this amygdalar circuit—has been shown to be involved in controlling feeding behavior [45] [46]. In particular, the nucleus appears to integrate food hedonic values [47] [48] and to influence searching and consumption of palatable food through a pathway involving opioidergic neurotransmission [48] [49]. In the context of feeding behavior, it is also particularly relevant to point out that, according to the present findings, the rlPAG is also in a position to integrate visceral and gustatory information from the visceral and gustatory cortical areas, and to a lesser degree, from the parabrachial area [50]. "
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    ABSTRACT: Previous studies have shown that a particular site in the periaqueductal gray (PAG), the rostrolateral PAG, influences the motivation drive to forage or hunt. To have a deeper understanding on the putative paths involved in the decision-making process between foraging, hunting, and other behavioral responses, in the present investigation, we carried out a systematic analysis of the neural inputs to the rostrolateral PAG (rlPAG), using Fluorogold as a retrograde tracer. According to the present findings, the rlPAG appears to be importantly driven by medial prefrontal cortical areas involved in controlling attention-related and decision-making processes. Moreover, the rlPAG also receives a wealth of information from different amygdalar, hypothalamic, and brainstem sites related to feeding, drinking, or hunting behavioral responses. Therefore, this unique combination of afferent connections puts the rlPAG in a privileged position to influence the motivation drive to choose whether hunting and foraging would be the most appropriate adaptive responses.
    Neural Plasticity 02/2009; 2009:612698. DOI:10.1155/2009/612698 · 3.60 Impact Factor
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    • "Regarding the functional roles of this amygdalar system , it is well known that the central nucleus—the main output way station of the circuit—is involved in controlling feeding behavior (Minano et al., 1992; Kask and Schioth, 2000). In particular, the nucleus appears to integrate food hedonic values (Glass et al., 2000; Pomonis et al., 2000) and to influence searching and consumption of palatable food (Hitchcott and Phillips, 1998; Pomonis et al., 2000). In line with this view, the larger mobilization of this amygdalar system during insect predation may be reflecting, at least partly, the higher palatability of the prey as compared with regular chow. "
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    ABSTRACT: The study of the neural basis of predatory behavior has been largely neglected over the recent years. Using an ethologically based approach, we presently delineate the prosencephalic systems mobilized during predation by examining Fos immunoreactivity in rats performing insect hunting. These results were further compared with those obtained from animals killed after the early nocturnal surge of food ingestion. First, predatory behavior was associated with a distinct Fos up-regulation in the ventrolateral caudoputamen at intermediate rostro-caudal levels, suggesting a possible candidate to organize the stereotyped sequence of actions seen during insect hunting. Insect predation also presented conspicuous mobilization of a neural network formed by a distinct amygdalar circuit (i.e. the postpiriform-transition area, the anterior part of cortical nucleus, anterior part of basomedial nucleus, posterior part of basolateral nucleus, and medial part of central nucleus) and affiliated sites in the bed nuclei of the stria terminalis (i.e. the rhomboid nucleus) and in the hypothalamus (i.e. the parasubthalamic nucleus). Accordingly, this network is likely to encode prey-related motivational values, such as prey's odor and taste, and to influence autonomic and motor control accompanying predatory eating. Notably, regular food intake was also associated with a relatively weak Fos up-regulation in this network. However, during regular surge of food intake, we observed a much larger mobilization in hypothalamic sites related to the homeostatic control of eating, namely, the arcuate nucleus and autonomic parts of the paraventricular nucleus. Overall, the present findings suggest potential neural systems involved in integrating prey-related motivational values and in organizing the stereotyped sequences of action seen during predation. Moreover, the comparison with regular food intake contrasts putative neural mechanisms controlling predatory related eating vs. regular food intake.
    Neuroscience 02/2005; 130(4):1055-67. DOI:10.1016/j.neuroscience.2004.10.020 · 3.33 Impact Factor
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