Dietary fat ingestion activates β‐endorphin neurons in the hypothalamus

Matsumura, Shigenobu; Eguchi, Akiyo; Okafuji, Yoko; Tatsu, Sotaro; Maekawa, Takafumi; Tsuzuki, Satoshi; Inoue, Kazuo; Fushiki, Tohru

doi:10.1016/j.febslet.2012.03.028

Cited by 26 publications

(17 citation statements)

References 16 publications

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“…Moreover, this role is consistent with the fact that POMC neurons and the opioid system are involved in the regulation of energy homeostasis (14)(15)(16)(17). The POMC neuron can be activated by ingestion of fat but cannot be sufficiently activated by intragastric administration of fat (5). It has also been reported that naltrexone administration can reduce sucrose intake even in animals that have been esophagostomized to prevent post-ingestive effects (24).…”

Section: Discussionsupporting

confidence: 76%

“…We recently reported that fat ingestion induces elevations in the endogenous opioid peptide, beta-endorphin, in cerebrospinal fluid (4). Furthermore, we have also demonstrated that fat ingestion can activate pro-opiomelanocortin (POMC) neurons in the hypothalamus, which synthesize beta-endorphin (5). Many reports have suggested that administration of opioid receptor antagonists can attenuate fat preference, an observation that is consistent with our findings (4,(6)(7)(8).…”

supporting

confidence: 91%

“…In particular, the glossopharyngeal nerve contributes to preference behavior associated with high concentrations of fat, since glossopharyngeal nerve transection (GLX) can partially inhibit POMC neurons that have been activated by fat ingestion (5). Conversely, olfactory nerve transection (ONX) can abolish the preference for low fat concentrations (18); thus, olfactory and gustatory transduction related to fat preference might rely on fat concentration in a different manner.…”

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confidence: 99%

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Mechanisms Involved in Guiding the Preference for Fat Emulsion Differ Depending on the Concentration

Sakamoto

Matsumura

Okafuji

et al. 2015

J Nutr Sci Vitaminol

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Most animals, including humans, have a high avidity for consuming dietary fat. Previous studies have reported that fat preference can be attributed to many factors, including palatable flavor, texture, and chemical perception. Moreover, transection of nerves associated with either olfaction or gustation (i.e., olfactory or glossopharyngeal nerve) has been shown to decrease fat ingestion (1-3). In the central nervous system, several studies have suggested that the opioid system, canonically associated with reward circuitry, is associated with dietary preferences for fat. We recently reported that fat ingestion induces elevations in the endogenous opioid peptide, beta-endorphin, in cerebrospinal fluid (4). Furthermore, we have also demonstrated that fat ingestion can activate pro-opiomelanocortin (POMC) neurons in the hypothalamus, which synthesize beta-endorphin (5). Many reports have suggested that administration of opioid receptor antagonists can attenuate fat preference, an observation that is consistent with our findings (4,(6)(7)(8).A significant amount of experimental evidence implicates the opioid system in the reward and reinforcement of drug addiction. We previously demonstrated that, similar to drug administration, fat ingestion can serve as a reinforcer by inducing place preference or strong lever-pressing behavior in mice (we define these as "reinforcing effects") (9, 10). Moreover, it has been reported that opioid receptor antagonists can diminish the reinforcing influence of fat (11). These findings suggest that the opioid system contributes not only to fat preference, but also to reinforcement. However, the concentration of fat that produces a reinforcing effect might differ from that inducing preference behavior. Indeed, while mice prefer fat even at low concentrations (12), the reinforcing property of fat is only observed in response to substances with higher fat content (13). These findings indicate that the mechanisms underlying preference for fat are distinctly dependent on fat content. Since POMC neurons regulate energy homeostasis modulating feeding and/or energy expenditure (14-17), the opioid system might have an influence on the preference for high fat concentrations.It also seems likely that several nerves (i.e., the chorda tympani, glossopharyngeal, and trigeminal nerves) are involved in recognizing the presence of dietary fat in the oral cavity. In particular, the glossopharyngeal nerve contributes to preference behavior associated with high concentrations of fat, since glossopharyngeal nerve transection (GLX) can partially inhibit POMC neurons that have been activated by fat ingestion (5). Conversely, olfactory nerve transection (ONX) can abolish the preference for low fat concentrations (18); thus, olfactory and gustatory transduction related to fat preference might rely on fat concentration in a different manner. Summary High-fat foods tend to be palatable and can cause addiction in mice via a reinforcing effect. However, mice showed preference for low fat concentrations that do not...

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Section: Discussionsupporting

confidence: 76%

supporting

confidence: 91%

mentioning

confidence: 99%

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Mechanisms Involved in Guiding the Preference for Fat Emulsion Differ Depending on the Concentration

Sakamoto

Matsumura

Okafuji

et al. 2015

J Nutr Sci Vitaminol

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“…16−19) However, pro-opiomelanocortin neurons, which release β-endorphin, are more strongly activated after fat ingestion compared to sucrose ingestion. 20) Similarly, the orexigenic or anorexigenic effects of opioid receptor agonists or antagonists are stronger in mice fed a high-fat diet than in those fed a highcarbohydrate diet. 21,22) These reports suggest that the opioid system is highly involved in the ingestion of dietary fat compared to sucrose.…”

Section: 2)mentioning

confidence: 99%

The opioid system majorly contributes to preference for fat emulsions but not sucrose solutions in mice

Sakamoto

Okahashi

Matsumura

et al. 2015

Bioscience, Biotechnology, and Biochemistry

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Rodents show a stronger preference for fat than sucrose, even if their diet is isocaloric. This implies that the preference mechanisms for fat and sucrose differ. To compare the contribution of the opioid system to the preference of fat and sucrose, we examined the effects of mu-, delta-, kappa-, and non-selective opioid receptor antagonists on the preference of sucrose and fat, assessed by a two-bottle choice test and a licking test, in mice naïve to sucrose and fat ingestion. Administration of non-selective and mu-selective opioid receptor antagonists more strongly inhibited the preference of fat than sucrose. While the preference of fat was reduced to the same level as water by the antagonist administration that of sucrose was still greater than water. Our results suggest that the preference of fat relies strongly on the opioid system, while that of sucrose is regulated by other mechanisms in addition to the opioid system.

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“…It has been reported that several factors, including texture, flavor, orosensory chemical detection of fats, and postingestive effects, might contribute to food palatability. [1][2][3][4][5][6][7] Among these, the flavor of fats is considered to play an important role in increasing palatability. [8][9][10][11] Dietary fats contain many types of flavors.…”

mentioning

confidence: 99%