NEURAL and METABOLIC CONTROL of MACRONUTRIENT INTAKE Edited by Hans-Rudolf Berthoud, Ph.D. Randy J. Seeley, Ph.D. CRC PR ESS Boca Raton London New York Washington, D.C. © 2000 by CRC Press LLC 2752_ fm_frame Page 2 Friday, September 3, 1999 4:18 PM Library of Congress Cataloging-in-Publication Data Neural and metabolic control of macronutrient intake / edited by Hans -Rudolf Berthoud, Randy J. Seeley. p. cm. Includes bibliographical references and index. ISBN 0-8493-2752-0 (alk. paper) 1. Appetite. 2. Food preferences. 3. Nutrition--Psychological aspects. 4. Neuropsychology. I. Berthoud, Hans-Rudolf. II. Seeley, Randy J. [DNLM: 1. Nutrition. 2. Dietary Carbohydrates--metabolism. 3. Dietary Fats--metabolism. 4. Dietary Proteins--metabolism. 5. Food Preferences--physiology. 6. Food Preferences--psychology. QU 145 N494 1999] QP136.N47 1999 612.3′9--dc21 DNLM/DLC for Library of Congress 99-29233 CIP This book contains information obtained from authentic and highly regarded sources. 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Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation, without intent to infringe. © 2000 by CRC Press LLC No claim to original U.S. Government works International Standard Book Number 0-8493-2752-0 Library of Congress Card Number 97-24341 Printed in the United States of America 1 2 3 4 5 6 7 8 9 0 Printed on acid-free paper 2752_ fm_frame Page 3 Friday, September 3, 1999 4:18 PM Preface Several years ago the idea for this book grew out of a conversation at the European Winter Conference on Brain Research. Over a beer, the two editors of this book were discussing the topic of macronutrient selection and the potential involvement of the brain in its control. Macronutrient selection refers to the process by which general omnivores choose to consume differing amounts of protein, carbohydrate, or fats in their diets. Considerable controversy still surrounds to what degree macronutrient content of particular foods guides ingestive behavior. While neither of us had done a tremendous amount of research on macronutrient selection, over the course of several beers we began a spirited “discussion” of this topic. Quickly, however, we realized how difficult a topic it was to discuss because there was no resource that brought together the large and diverse literature related to macronutrient selection. That is to say, our arguments rapidly devolved because we lacked a way to resolve disputes over the current state of knowledge about issues related to macronutrient selection. Neither of us possessed the breadth of knowledge (from biochemistry to human and animal behavior) that a real consideration of these issues would require. Before we left that meeting, we decided that very few individuals likely had the necessary breadth of knowledge and therefore a book that could tie together the pieces of this intricate puzzle would be a valuable resource for individuals from a broad array of backgrounds with general interests in dietary selection. What you will find in this volume is our attempt to bring together chapters from the people who have most influenced current thinking on this topic. These individuals represent the truly interdisciplinary nature of this topic. They range from biochemists, nutritionists, psychologists, physiologists, neuroscientists, and molecular biologists. In addition to diverse backgrounds, the authors of these chapters are individuals who differ considerably on their opinions about the nature of macronutrient selection. We have gone to great lengths to put into this single volume chapters from people who clearly advocate the existence of separate control systems for the individual macronutrients and those who do not. In this way, we believe readers can evaluate these arguments for themselves. The book is arranged to provide three types of information. First, the basic background of the biochemical and physiological systems as they relate to macronutrient selection. Second, opinions and data concerning to what degree animals and humans show evidence of macronutrient selection. Third, evidence about how the central nervous system might be involved in the choices animals make among macronutrients. Few basic research problems with this level of controversy have such important practical implications. Increased consumption of dietary fat in developed countries is closely tied to increases in heart disease, diabetes, and obesity. If separate control systems exist, it leaves open the possibility that strategies could be devised to intervene in these control systems and alter the proportion of fat in the diet. If such separate control systems do not exist, such interventions will eventually fail. Consequently, the stakes of this particular debate both for basic understanding of how the brain controls ingestive behavior and for our ability to decrease the incidence of these dangerous condi- tions are extremely high. © 2000 by CRC Press LLC 2752_ fm_frame Page 5 Friday, September 3, 1999 4:18 PM The Editors Hans-Rudolf Berthoud was born near Zürich, Switzerland, and obtained his Diploma in Biology (1969) and Ph.D. in Neurobehavioral Biology and Physiology (1973) from the Swiss Federal Institute of Technology (ETH), Zürich. During his postdoctoral training, Dr. Berthoud continued to study the role of the hypothalamus in ingestive behavior with Gordon J. Mogenson at the University of Western Ontario in Canada, and then collaborated with Bernard Jeanrenaud and Albert Renold as “Chef de Traveaux” at the University of Geneva Medical School on projects focusing on the neural control of pancreatic secretion. In 1982 he emigrated to the U.S., where he began a long collaboration with Terry Powley at Purdue University investigating anatomy and physiology of the vagus nerve. In 1992 Dr. Berthoud was appointed Associate Professor at the Pennington Biomedical Research Center in Baton Rouge, and Louisiana State University Medical Center in New Orleans, LA, where he continued his studies on morphological, physiological, and behavioral aspects of vagal and central nervous mechanisms that control ingestive behavior and energy metabolism. Dr. Berthoud has published over 80 papers in leading journals, including several reviews and book chapters. He is a member of the Society for Neuroscience (SN), the American Physiological Society (APS), the Society for the Study of Ingestive Behavior (SSIB), the North American Association for the Study of Obesity (NAASO), and the International Society for Autonomic Nervous System Physiology (ISAN). Dr. Berthoud is on the Editorial Board for the American Journal of Physiology, Comparative and Regulatory Physiology, and Obesity Research. Randy J. Seeley received his undergraduate degree with honors from Grinnell College in 1989. He received his Ph.D. at the University of Pennsylvania in the Department of Psychology working with Dr. Harvey Grill. He then was a Post-Doctoral Fellow for 2 years working with Drs. Steve Woods and Dan Porte, Jr. at the University of Washington. He was also on the faculty of the Department of Psychology at the University of Washington for 2 years before moving to the University of Cincinnati in the fall of 1997. He was appointed as an Associate Professor in the Department of Psychiatry in the College of Medicine at the University of Cincinnati and a member of the Graduate Neuroscience Program, an Adjunct Associate Professor in the Department of Psychology, and Associate Director of the Obesity Research Center. Since 1993 he has coauthored over 60 papers and chapters concerning his work on the neural and metabolic control of food intake and body weight in rodent models including reviews in the New England Journal of Medicine and Science. He is on the editorial board for the American Journal of Physiology and a member of the Society for Neuroscience, Society for the Study of Ingestive Behavior, North American Association for the Study of Obesity, American Psychological Association, and American Psychological Society. © 2000 by CRC Press LLC 2752_ fm_frame Page 7 Friday, September 3, 1999 4:18 PM Contributors Karen Ackroff T. W. Castonguay Department of Psychology Department of Nutrition and Food Science Brooklyn College of CUNY University of Maryland Brooklyn, NY 11210 Marie Mount Hall College Park, MD 20742 Bernard Beck Mark Chavez INSERM U. 308 The Monell Chemical Senses Institute Mécanismes de Régulation du Comportement 3500 Market St. Alimentaire Philadelphia, PA 19104 38 rue Lionnois 54000 Nancy, France Jian Chen Pennington Biomedical Research Center Stephen C. Benoit Louisiana State University Department of Psychiatry 6400 Perkins Rd. University of Cincinnati College of Medicine Baton Rouge, LA 70808 P.O. Box 670559 Cincinnati, OH 45267-0559 Mihai Covasa Department of V.C.A.P.P. and Program in Hans-Rudolf Berthoud Neuroscience Neurobiology of Nutrition Laboratory College of Veterinary Medicine Pennington Biomedical Research Center Washington State University Louisiana State University Pullman, WA 99164 6400 Perkins Rd. T. L. Davidson Baton Rouge, LA 70808 Department of Psychological Sciences Charles J. Billington 1364 Psychological Sciences Bldg. Department of Psychiatry Purdue University Veterans Administration Medical Center West Lafayette, IN 47907-1364 Minneapolis, MN 55417 John M. de Castro Department of Psychology John E. Blundell Neuropsychology and Behavioral Neuroscience Biopsychology Group Program School of Psychology Georgia State University University of Leeds University Plaza Leeds, LS2 9JT, U.K. Atlanta, GA 30303 David A. Booth Ambrose A. Dunn-Meynell Nutritional Psychology Research Group Department of Neurosciences University of Birmingham Neurology Service, VA Medical Center Birmingham B15 2TT, England East Orange, NJ 07018 Lynda M. Brown J. P. Flatt Department of Nutrition and Food Science Department of Biochemistry and Molecular University of Maryland Biology Rm. 3304, Marie Mount Hall University of Massachusetts Medical Center College Park, MD 20742 Worcester, MA 01655 © 2000 by CRC Press LLC 2752_ fm_frame Page 8 Friday, September 3, 1999 4:18 PM Louis A. Foster Leigh Anne Howell Department of Anatomy and Physiology Pennington Biomedical Research Center College of Veterinary Medicine Louisiana State University Kansas State University 6400 Perkins Rd. Manhattan, KS 66506 Baton Rouge, LA 70808 Frank H. Koegler Mark I. Friedman Oregon Regional Primate Research Center The Monell Chemical Senses Institute Oregon Health Sciences University 3500 Market St. 505 N.W. 185th Ave. Philadelphia, PA 19104 Beaverton, OR 97006 K. Fukagawa Wolfgang Langhans Department of Internal Medicine Institute of Animal Sciences Oita University Group of Physiology and Animal Husbandry Swiss Federal Institute of Technology (ETH) Bennett G. Galef, Jr. Zurich, 8092 Switzerland Department of Psychology McMaster University Sarah F. Leibowitz Hamilton, ON L8S 4K1 Canada The Rockefeller University 1230 York Ave. Kyriaki Gerozissis New York, NY 10021 Physiopathologie de la Nutrition Barry E. Levin CNRS ESA 7059 Department of Neurosciences Universite Paris 7, 2 Place Jussieu Neurology Service, 127C VA Medical Center 75251 Paris Cedex 05, France East Orange, NJ 07009 Dorothy W. Gietzen Allen S. Levine Department of Anatomy, Physiology and Cell Department of Medicine Biology Veterans Affairs Medical Center School of Veterinary Medicine One Veterans Dr. University of California, Davis Research Service (151) Davis, CA 95616 Minneapolis, MN 55417 Michael J. Glass Ling Lin Minnesota Obesity Center Pennington Biomedical Research Center Department of Psychology Louisiana State University Veterans Affairs Medical Center 6400 Perkins Rd. Minneapolis, MN 55417 Baton Rouge, LA 70808 Tiffany D. Mitchell Jason C. G. Halford Pennington Biomedical Research Center University of Liverpool Louisiana State University Department of Psychology 6400 Perkins Rd. Eleanor Rathbone Building Baton Rouge, LA 70808 Liverpool, L6972A, U.K. Timothy H. Moran Ruth B. S. Harris Department of Psychiatry and Behavioral Pennington Biomedical Research Center Sciences Louisiana State University Johns Hopkins University School of Medicine 6400 Perkins Rd. 720 Rutland Ave., Ross Bldg., Rm. 618 Baton Rouge, LA 70808 Baltimore, MD 21205 © 2000 by CRC Press LLC 2752_ fm_frame Page 9 Friday, September 3, 1999 4:18 PM Javier R. Morell Edmund T. Rolls Department of Psychological Sciences University of Oxford 1364 Psychological Sciences Bldg. Department of Experimental Psychology Purdue University South Parks Rd. West Lafayette, IN 47907-1364 Oxford OX1 3UD England Stylianos Nicolaïdis Vanessa H. Routh Institut Europeen des Sciences du Gout et des Department of Pharmacology and Physiology Comportements Alimentaires New Jersey Medical School Universite de Bourgogne Newark, NJ 07103 21000 Dijon, France Donna H. Ryan Leona M. O’Reilly Pennington Biomedical Research Center Rowett Research Institute Louisiana State University Bucksburn, Aberdeen, Scotland AB21 9SB 6400 Perkins Rd. Baton Rouge, LA 70808 Martine Orosco Physiopathologie de la Nutrition Anthony Sclafani CNRS ESA 7059 Department of Psychology Universite Paris 7, 2 place Jussieu case 7126 Brooklyn College and the Graduate School 75251 Paris Cedex 05, France 75251 City University of New York 2900 Bedford Ave. David Raubenheimer Brooklyn, NY 11210 Department of Zoology and University Museum Randy J. Seeley of Natural History Department of Psychiatry University of Oxford University of Cincinnati South Parks Rd. P.O. Box 670559 Oxford, Ox1 3PS, U.K. Cincinnati, OH 45267-0559 Christine A. Riedy Stephen J. Simpson Department of Dental Public Health Department of Zoology and University Museum University of Washington of Natural History Seattle, WA University of Oxford South Parks Rd. Robert C. Ritter Oxford, Ox1 3PS, U.K. Department of V.C.A.P.P. and Program in Brenda K. Smith Neuroscience College of Veterinary Medicine Pennington Biomedical Research Center Washington State University Louisiana State University Pullman, WA 99164 6400 Perkins Rd. Baton Rouge, LA 70808 W. Sue Ritter Edward M. Stricker Department of Veterinary and Comparative Department of Neuroscience Anatomy, Physiology and Pharmacology 479 Crawford Hall Washington State University University of Pittsburgh Pullman, WA 99164-6520 Pittsburgh, PA 15260 Barbara J. Rolls R. James Stubbs Nutrition Department Human Nutrient Unit Pennsylvania State University Rowett Research Institute 226 Henderson Bldg. Greenburn Rd. University Park, PA 16802 Bucksburn, Aberdeen, Scotland AB21 9SB U.K. © 2000 by CRC Press LLC 2752_ fm_frame Page 10 Friday, September 3, 1999 4:18 PM Patrick Tso Michael Wiater Department of Pathology Department of Veterinary and Comparative University of Cincinnati Medical Center Anatomy, Physiology and Pharmacology 231 Bethesda Avenue (ML 0529) Washington State University Cincinnati, OH 45267-0529 P.O. Box 646520 Pullman, WA 99164-6520 Louise Thibault Stephen C. Woods School of Dietetics and Human Nutrition Department of Psychiatry Macdonald Campus of McGill University University of Cincinnati Medical Center 21.111 Lakeshore Rd. P.O. Box 670559 Ste. Anne de Bellevue, QC H9X 3V9 Canada Cincinnati, OH 45267-0559 Gertjan van Dijk David A. York Department of Animal Physiology Pennington Biomedical Research Center University of Groningen Louisiana State University Kerklaan 30 6400 Perkins Rd. Haren 9750AA The Netherlands Baton Rouge, LA 70808 Malcolm Watford Bradley D. Youngblood Department of Nutritional Sciences Pennington Biomedical Research Center Cook College Louisiana State University Rutgers University 6400 Perkins Rd. New Brunswick, NJ 08901 Baton Rouge, LA 70808 © 2000 by CRC Press LLC 2752_ fm_frame Page 11 Friday, September 3, 1999 4:18 PM Acknowledgments The authors would like to thank Stephen C. Woods for his input and guidance on the ideas and organization of this book. We would also like to thank Patricia James for administrative help. In particular the authors would also like to thank Becky Topmiller for her tireless efforts to keep us organized and fighting through the huge task of pulling all of these chapters together. We might have been able to do this book without her, but we know it would not have been any fun. © 2000 by CRC Press LLC 2752_ fm_frame Page 13 Friday, September 3, 1999 4:18 PM Contents Section I Evidence for macronutrient selection: basic mechanisms and strategies to achieve regulation Chapter 1 Specific Appetites and Homeostatic Systems Edward M. Stricker Chapter 2 Too Many Choices? A Critical Essay on Macronutrient Selection Mark I. Friedman Chapter 3 Is There a Specific Appetite for Protein? Bennett G. Galef, Jr. Chapter 4 Geometric Models of Macronutrient Selection Stephen J. Simpson and David Raubenheimer Chapter 5 Macronutrient Selection in Free-Feeding Humans: Evidence for Long-Term Regulation John M. de Castro Chapter 6 Macronutrient-Specific Hungers and Satieties and Their Neural Bases, Learnt from Pre- and Postingestional Effects of Eating Particular Foodstuffs David A. Booth and Louise Thibault Chapter 7 Macronutrient-Conditioned Flavor Preferences Anthony Sclafani Chapter 8 Evidence for Caloric, but Not Macronutrient, Compensation to Preloads Varying in Fat and Carbohydrate Content in Human Subjects Barbara J. Rolls and Timothy H. Moran Chapter 9 The Effects of Nutrient Preloads on Subsequent Macronutrient Selection in Animal Models L. A. Foster © 2000 by CRC Press LLC
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