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EDITORIAL FOCUS
APPETITE, OBESITY, DIGESTION, AND METABOLISM
Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health, Baltimore, Maryland
WHAT IS IT THAT IS habit-forming about food? Sweet foods and fatty foods are habit-forming and sweet-fatty foods perhaps more than doubly so. Many kitchen and industrial experiments have gone into the determination of the amounts of sugar and butter to optimize the palatability of a given meal or substance. But humans also seek out bitter and tart substances. Cattle seek out and ingest alfalfa, which is indigestible and, interestingly, not very tasty for monogastric animals, such as humans or pigs. What is really known about the elements of orosensory rewards? We know the sweeter the better but that sour, salt, and bitter tastes are accepted only at low concentration and rejected at high concentration (14). What about foodstuffs that are not identified by the four tastes or, as in the case of corn oil, even by olfaction (17)? New data of Liang et al. (9) suggest an answer to this important question.
Because flavorless water is rewarding for thirsty animals, the identification of the rewarding quality of fluids offers an easier case and an instructive example. It is the oral cooling that accompanies ingested water that makes it rewarding. As is well known from personal experience, cool water is preferred to warm (4, 15). Attribution of reward to this sensory property rather than to postingestional effects of rehydration, however, like attribution of sucrose reward to sweetness (5) rather than to the effects of sugars on memory consolidation (12), requires more than correlative data. The critical test involves dissociation of the orosensory and postingestional properties of the tastant. In the case of hydrational rewards, several studies confirm that oral cooling, even without consequent hydration, is the rewarding consequence of drinking. Water-deprived (but not sated) rodents will persistently lick a cool airstream (despite the fact that it further dehydrates the animal by evaporating the animal's saliva) and this air licking will reduce subsequent drinking of and working for real water (3, 6). Thirsty rats will even lick an airstream that is warm, so long as the warm air is dry and will cool the oral cavity by evaporating saliva (3). Thus oral cooling is the immediate reward for drinking in thirsty rats (10, 11).
A more direct way to separate the orosensory and postingestional effects of ingested rewards is to disconnect the oral cavity from the digestive cavity. The simplest approximation of disconnection involves a gastric fistula that can be opened to allow an ingested tastant to flow out of the stomach without significant absorption. Using this method, Hajnal et al. (5) have confirmed a conclusion reached decades earlier from studies of nonnutritive sweeteners (16); sweetness itself is a reinforcer, independent of the postingestive ability of sugars to enhance memory consolidation (12).
The mechanism by which nonnutritive sweeteners (or sugar solutions that are allowed to drain through a gastric fistula) can reinforce learning and establish response habits is not really understood. Formal theories of reinforcement stress the enhancement of memory consolidation as the essence of the mechanism for stamping in memory (8, 13). It is known that glucose given subcutaneously following a learning trial can improve retention of what was learned in the trial. This posttrial memory-consolidation effect suggests that the postingestional effects of glucose are reinforcing. While this may be true, some additional reinforcing action must be caused by sweet taste itself; nonnutritive saccharin is reinforcing (16), as is sham-fed sucrose (open gastric fistula) (2).
If sweet taste is a sufficient condition for food reward, what is the mechanism? Just as posttrial glucose can enhance consolidation of recently formed memories, so can posttrial amphetamine (1, 7). The memory-enhancing effects of posttrial amphetamine appear to result from the release of dopamine caused by the drug (18). Thus the ability of sham-fed sucrose to elevate brain dopamine levels may account for the rewarding effects of sweet taste.
Liang et al. (9) show that rats ingesting corn oil without the opportunity to digest it show elevations of nucleus accumbens dopamine that are comparable to those seen in rats ingesting sucrose. Thus the rewarding effects of lipids appear to activate a similar reward mechanism, but by very different sensory pathways, as do rewarding sugars. The study of Liang et al. takes us beyond the microstructure of feeding to the microstructure of oral rewards, a much-needed approach for advancement of our understanding of ingestive behavior.
FOOTNOTES
Address for reprint requests and other correspondence: R. A. Wise, Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health, Baltimore, Maryland 21224 (e-mail: rwise{at}mail.nih.gov)
REFERENCES
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