Peripheral Gustatory Processing of Free Fatty Acids

It is well known that obesity is a major health problem, with approximately 66% of adults in the United States considered overweight and more than 1 billion overweight adults worldwide (Ogden et al., 2006) (World Health Organization). In addition to the impact on the joints and bones caused by increased body mass, obesity can also lead to heart disease, hypertension, diabetes, and stroke (Wong and Marwick, 2007). Given the severity and consequences of these conditions, it is not surprising that there is a large body of research exploring factors that contribute to the development of obesity, including diet and, more specifically, the proportion of certain foods in the diet. Vilified in the media as “Public Enemy Number One in the Battle of the Bulge,” dietary fat, and in particular the over consumption of fat, is considered by many to be the greatest contributing factor to obesity. Yet, is fat the enemy? Clearly, high fat ingestion, along with lack of exercise, has the potential to negatively impact a healthy lifestyle. At the same time, however, fats are critical for many biological processes. As the lipid bilayer of cells, fat is a building block for life and, in the form of myelin, enables fast electrical communication between neurons. Fat provides insulation that helps conserve body heat in cold climates and also can protect organs, like those necessary for reproduction, from damage. Fats and the main component of fats, free fatty acids, are essential for the growth and development of vital organs, including the brain (Spector, 2001). Clearly, fat is crucial for life, yet the body cannot synthesize certain kinds of fats. Rather, these fats are obtained from ingested food. Thus, the ability to detect certain kinds of fat in food sources is necessary for survival. Fortunately, there is strong motivation to find and subsequently consume fat because fat is preferred by many animals, including humans. What is it about fat that is so alluring? In the past, the palatability of fat was thought to be the result of smell and/or texture. For example, impairment of the ability to smell (either by bilateral transection of the olfactory nerve or by destruction of the olfactory mucosa with ZnSO) eliminates the preference for high-fat foods in mice (Mela, 1988; Kinney and Antill, 1996). Moreover, increasing the texture of low-fat dairy products also increases the perceived fat content. Interestingly, sensitivity to the texture of fat seems to be related to the number of functional taste buds on the tongue, as people with the greatest number of taste buds (i.e., so-called “super tasters”) are the best at discriminating between solutions with varying fat contents (Bartoshuk et al., 1994). Moreover, there are even cells in a specialized primate brain area called the orbitofrontal cortex that respond only to the texture of fats (Verhagen et al., 2003). Clearly, smell and texture are important for fat perception. However, rats can discriminate between different kinds of oils that, presumably, have a similar texture and continue to prefer fat solutions when texture and smell are minimized in behavioral tests (Larue, 1978; Fukuwatari et al., 2003). Furthermore, ingested fats are rapidly (within 1–5 s) broken down into free fatty acids in the oral cavity by lingual lipase (Kawai and Fushiki, 2003). In fact, rats have a robust preference for free fatty acids; however, prevention of the breakdown of fats into free fatty acids by the addition of a lingual lipase inhibitor greatly reduces rats’ preference for fat solutions. Thus, fat and in particular the building blocks of fats—free fatty acids—have a taste component that plays a strong role in our fat preference.