Blood Glucose Patterns and the Control of Feeding Behavior: A New Framework for the Control of Meal Initiation
A new framework for understanding the control of feeding behavior, with special emphasis on the evolution of hunger, the initiation of feeding, and its dependence on patterns of blood glucose, is the subject of this chapter. A perspective on the current status and future directions of this search for a more complete understanding of the regulation of feeding behavior in laboratory rats and humans is presented, including theoretical and experimental components. Experimental evidence supports the hypothesis that spontaneous, self-resolving transient declines in blood glucose precede and signal meal initiation in nondeprived, free-feeding rats and time-isolated humans. This signal precedes food-seeking behavior and the initiation of a meal but does not predict the size of the meal or the timing of meal termination. The precise antecedent conditions required, in terms of the shape of the transient declines in blood glucose, for meal initiation or meal requests have been defined. This is followed by a statement and overview of a signal detection and pattern recognition theory of the control of meal initiation. The current working hypothesis that transient declines in blood glucose are endogenous metabolic patterns that are represented in the central nervous system is then presented. These patterns are detected and recognized by the central nervous system and are mapped into meal initiation in rats and are correlated with meal requests in humans. The distinguishing feature of the theory is that it is the temporal pattern, shape, or waveform of blood glucose dynamics – rather than the glucose molecule, or the absolute decrease in blood glucose, or blood glucose concentration, or glucose utilization – that is detected and contains critical information that is extracted by the central nervous system to control meal initiation. Then, the experimental studies on meal initiation and its dependence on patterns of blood glucose in humans are reviewed. An association between transient declines in blood glucose concentration and meal requests and changes in hunger ratings in human subjects isolated from food and time cues has been demonstrated. This association was observed following both spontaneous and insulin-induced transient declines in blood glucose. These results support and strengthen the conclusion that the transient decline in blood glucose represents a temporal pattern that reflects an antecedent physiological event or provides a signal related to the expression of hunger in humans. Finally, the implications for the understanding of the control of feeding behavior and the regulation of energy balance are discussed.
KeywordsBlood Glucose Feeding Behavior Blood Glucose Concentration Transient Decline Maintain Glucose Homeostasis
Central nervous system
Glucose disposal rate
Glucose production rate
Transient declines in blood glucose
The ideas, concepts, and implications of the experimental results discussed here have been strongly influenced by the experimental approach, seminal integrative perspectives, major concepts, and brilliant insights into the regulation of feeding of Jacques Le Magnen, Director of the Laboratoire de Neurophysiologie Sensorielle et Comportementale, College de France in Paris, France, who died in May 2002.
The participation of Peter Brandon, Kathy Kamp, Brian Clarke, Debra Driscoll, Debra Howell, Kim Moore, Mary Lisa Sassano, Garry Mackie, Joe Sia, Dino Micholaidis, Caroline Hoffman, Michael Rosenbaum, and Kalthleen Melanson in many of these studies is gratefully acknowledged. We also acknowledge Stephen Woods, Donald Novin, John Blundell, Harvey Weingarten, France Bellisle, Jeanine Louis-Sylvestre, Christiane Achagiotis, Luc Penicaud, Harvey Grill, Joel Kaplan, Randall Sakai, Randy Seeley, Gerry Smith, Rudolph Leibel, Jules Hirsch, Margriet Westerterp, and Wim Saris for their interest, comments, suggestions, encouragement, and many helpful discussions.
The human research was supported, in part, by National Institutes of Health Grants RR-00102 (to the Clinical Research Center, Rockefeller University), DK-01983, and DK-30583.
Address for reprint requests and other correspondence: L. Arthur Campfield, Department of Food Science and Human Nutrition, Colorado State University, Fort Collins, CO 80523–1571 (E-mail: email@example.com)
- Booth DA. In: Booth DA, ed. Hunger models. London: Academic; 1978. p. 227–78.Google Scholar
- Campfield LA, Smith FJ. Int J Obesity. 1990a;14:15–33.Google Scholar
- Campfield LA, Smith FJ. In: Bray GA, ed. Bailliere’s clinical endocrinology and metabolism. London: Bailliere Tindal; 1999. p. 13–30.Google Scholar
- Damasio A. Looking for spinoza: joy, sorrow and the feeling brain. New York: Harcourt; 2003.Google Scholar
- Le Magnen J. Hunger. London: Cambridge University Press; 1985.Google Scholar
- Le Magnen J. Neurobiology of feeding and nutrition. San Diego: Academic; 1992.Google Scholar
- Nicolaidis S. Proc IUPS. 1974;26:122–3.Google Scholar
- Nicolaidis S, Even P. Compte Rendu Sci Acad Sci. 1984;298:295–300.Google Scholar
- Ritter S, Taylor JS. Am J Physiol Regul Integr Comp Physiol. 1990;258:R1395–401.Google Scholar
- Smith FJ, Campfield LA. Am J Physiol Regul Integr Comp Physiol. 1993;265:R1423–9.Google Scholar
- VanItallie TB. Int J Obesity. 1990;14:1–10.Google Scholar
- VanItallie TB, Hashim SA. Am J Clin Nutr. 1960;8:587–94.Google Scholar
- VanItallie TB, Beaudoin R, Mayer J. J Clin Nutr. 1953;1:208–16.Google Scholar