Research ReviewAnticipatory physiological regulation in feeding biology: Cephalic phase responses
Introduction
Appetite, food preferences, and the regulation of food intake are key aspects of energy balance and weight homeostasis. There is an ever growing list of peptides, receptors, and other gene products associated with appetite and the regulation of food intake, and investigating their interrelated roles is an important process for understanding the proximate mechanisms by which people decide when and what to eat, and when to stop. In our opinion, a comparative, evolutionary perspective will also be important to understanding why the imbalance between food intake and energy expenditure appears to be so refractory.
The acquisition of food is a necessity for animals. Strong selective pressures have acted to produce the anatomy, physiology, and behavior that serve to enhance an animal's ability to ingest, digest, absorb, and ultimately metabolize the nutrients necessary for survival and reproduction. There are anticipatory physiological responses to feeding, the cephalic phase responses, that set in motion digestive and endocrine cascades that increase the efficiency of digestion and metabolism, but also directly and indirectly regulate meal size and duration. These cephalic phase responses can be conditioned, so experience, learning, and hence social and cultural factors, can and will play a role in their expression.
In this paper, we examine the role of cephalic phase responses in the regulation of food intake. The term cephalic phase response refers to anticipatory physiological regulation related to food and feeding; i.e. digestive and metabolic responses to food cues generated by the central nervous system that prepare the organism to ingest, digest, absorb, and metabolize food (Pavlov, 1902; Powley, 1977; Smith, 1995). These anticipatory physiological responses increase the efficiency with which an organism utilizes food. One result is an increase in the amount of food that can be processed at a given time; an advantage in our past evolutionary history, but possibly a source of our species’ susceptibility to obesity in the modern milieu. Recent evidence suggests that physiological responses that serve to end feeding also can have a cephalic phase. Thus, by the first bite of food, or even before, physiological processes have been set in motion that will influence the duration of the meal and the amount of food eaten (Smith, 2000).
We will examine cephalic phase responses from an adaptive perspective. We focus on the functions of various cephalic phase responses, their effects on food intake, and the possible selective pressures that have influenced their evolution.
Section snippets
Importance of anticipatory responses in regulatory physiology
Animals anticipate. Behavior, physiology, and metabolism are not merely reactive. The senses convey information about the external environment to the central nervous system. The central nervous system interprets this information within the constraints of experience (knowledge), intrinsic, evolved tendencies (phylogeny), and current conditions (e.g. social setting, nutritional status, and so forth). Is there a threat? Is there an opportunity? The central nervous system sends messages to the
Importance of anticipatory responses in feeding biology
Human beings feed in discrete meals. In consequence, food enters our bodies in pulses, and presents our digestive and metabolic systems with challenges to accommodate a discontinuous supply of nutrients (Storlien, Oakes, & Kelley, 2004 Storlien et al., 2004). Our internal milieu is not strictly constant. The state of the digestive system and numerous other organ systems (e.g. liver, kidney, adipose tissue) constantly change to accommodate conditions of nutrient excess (feeding) followed by
Cephalic phase responses
The concept was first introduced by Pavlov in his work on the alimentary tract and its secretions. The phrase originally used by Pavlov was “psychic secretions” (see Powley, 1977; Smith, 1995; Todes, 2002). For Pavlov, salivary secretions were digestive secretions, serving the same intrinsic function as gastric and intestinal secretions—enabling the animal to utilize food for bodily needs. He demonstrated in dogs that salivation varied with the food ingested. For example that ingesting dry food
Evidence for cephalic phase responses
There is a considerable literature on cephalic phase responses, going back to Pavlov (Todes, 2002). Cephalic phase responses have been demonstrated in a wide range of birds and mammals, including humans, nonhuman primates, dogs, cats, sheep, rabbits, and rats (Powley, 1977). Their origin would appear to be quite ancient; for example striped bass display cephalic phase insulin and glucagon responses (Papatryphon, Capilla, Navarro, & Soares, 2001 Papatryphon et al., 2001). Some of these cephalic
Cephalic phase insulin response
Insulin is the primary peptide regulating glucose metabolism. Insulin increases glucose storage (in the form of glycogen) in liver and muscle, decreases lipolysis and gluconeogenesis, and increases fatty acid synthesis by adipose tissue (Porte, Baskin, & Schwartz, 2005 Porte et al., 2005). The net result is to lower blood glucose concentration by increasing the conversion of glucose to other energy storage molecules (glycogen and fat) and decreasing the production of glucose from the liver.
In
Evidence for central nervous system contribution
Responses to food cues can be both intrinsic and learned (Booth, 1972; Rozin, 1976). Conditioned taste preferences and conditioned taste aversions provide strong proof that responses to food cues can be learned and modified. For example, most animals readily learn to avoid foods that render them ill; a special visceral learning linked to food ingestion (Garcia, Hankins, & Rusiniak, 1974 Garcia et al., 1974; Rozin, 1976). Bait shyness linked to poison is well known and is an important adaptation
The paradox of feeding
Cephalic phase responses serve postabsorptive metabolism and physiology as well as digestion. They prepare the organism to assimilate the ingested nutrients. This is a key adaptation, as although feeding is necessary for survival, it also presents a significant challenge to homeostasis, in what has been termed the paradox of feeding (Woods, 1991).
The homeostatic paradigm has guided thought and research on physiology for over one hundred years. Starting from the work of Bernard (1865) to Cannon
A role for cephalic phase responses in appetite and satiety?
Cephalic phase responses have been suggested to play a role in appetite and satiety (Powley, 1977; Woods, 1991). Palatable foods generally result in more robust cephalic phase responses than do less preferred foods. Preventing cephalic phase responses results in animals and humans eating smaller meals (reviewed in Woods, 1991). This is an example of the short-term effects of cephalic phase responses and the role of defense of homeostasis in appetite and satiety. Cephalic phase responses would
Diverse actions in diverse tissues
Leptin provides an example of a key concept we believe needs emphasizing in regulatory physiology. More and more, physiologically important peptides, steroids, and other information molecules are being shown to have multiple functions in diverse tissues. Their actions and regulation can be tissue and context specific. Leptin, for example, is secreted by placenta and appears to have important functions in fetal development (Bajari, Nimpf, & Schneider, 2004 Bajari et al., 2004; Henson &
Evolutionary considerations
Physiological and metabolic systems serve the survival and reproductive capabilities of the organism (fitness). Anticipatory physiological regulation is an adaptive strategy that enables animals to respond faster to physiologic and metabolic challenges. The cephalic phase responses are anticipatory responses that prepare animals to digest, absorb and metabolize nutrients. They enable the sensory aspects of the food to interact with the metabolic state of the animal to influence feeding
Acknowledgment
Partial funding was provided to MLP by US PHS Grant R01 DK077639.
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