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FAT DETECTION
TASTE, TEXTURE, AND POST INGESTIVE EFFECTS
Edited by
Jean-Pierre Montmayeur, Ph.D.
Centre National de la Recherche Scientifique
Dijon, France
Johannes le Coutre, Ph.D.
Nestlé Research Center
Lausanne, Switzerland
Boca Raton London New York
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Library of Congress Cataloging-in-Publication Data
Fat detection : taste, texture, and post ingestive effects / editors, Jean-Pierre Montmayeur
and Johannes le Coutre.
p. ; cm. -- (Frontiers in neuroscience)
Includes bibliographical references and index.
ISBN 978-1-4200-6775-0 (hardcover : alk. paper)
1. Taste. 2. Food--Fat content. 3. Food preferences. 4. Lipids in human nutrition. I.
Montmayeur, Jean-Pierre. II. le Coutre, Johannes. III. Series: Frontiers in neuroscience
(Boca Raton, Fla.)
[DNLM: 1. Taste Perception--physiology. 2. Dietary Fats--adverse effects. 3. Dietary
Fats--metabolism. 4. Food Preferences--physiology. 5. Taste--physiology. WL 702 F252
2010]
QP456.F38 2010
612.8’7--dc22 2009012412
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Contents
Series Preface ............................................................................................................xi
Foreword ................................................................................................................ xiii
Preface...................................................................................................................... xv
Editors .....................................................................................................................xix
Contributors ............................................................................................................xxi
PART I Importance of Dietary Fat
Chapter 1 Evolutionary Perspectives on Fat Ingestion
and Metabolism in Humans ..................................................................3
William R. Leonard, J. Josh Snodgrass, and Marcia L. Robertson
Chapter 2 Pathophysiology and Evolutionary Aspects of Dietary Fats
and Long-Chain Polyunsaturated Fatty Acids across
the Life Cycle...................................................................................... 19
Frits A.J. Muskiet
PART II Taste of Fat: From Detection
to Behavior
Chapter 3 Gustatory Mechanisms for Fat Detection ........................................... 83
Timothy A. Gilbertson, Tian Yu, and Bhavik P. Shah
Chapter 4 Role of the Gustatory System in Fatty Acid Detection in Rats ........ 105
David W. Pittman
Chapter 5 Peripheral Gustatory Processing of Free Fatty Acids ...................... 123
Jennifer M. Stratford and Robert J. Contreras
Chapter 6 Orosensory Factors in Fat Detection ................................................ 137
James C. Smith
vii
viii Contents
Chapter 7 Fat Taste in Humans: Is It a Primary?............................................. 167
Richard D. Mattes
PART III Neural Representations
of Dietary Fat Stimuli
Chapter 8 Neural Representation of Fat Texture in the Mouth........................ 197
Edmund T. Rolls
Chapter 9 Advantageous Object Recognition for High-Fat Food Images ....... 225
Ulrike Toepel, Jean-François Knebel, Julie Hudry,
Johannes le Coutre, and Micah M. Murray
PART IV Sensory Appeal of the Fat-Rich Diet
Chapter 10 Preference for High-Fat Food in Animals ...................................... 243
Yasuko Manabe, Shigenobu Matsumura, and Tohru Fushiki
Chapter 11 Human Perceptions and Preferences for Fat-Rich Foods................ 265
Adam Drewnowski and Eva Almiron-Roig
PART V Control of Food Intake
as a Function of Fat
Chapter 12 Oral and Postoral Determinants of Dietary Fat Appetite ............... 295
Karen Ackroff and Anthony Sclafani
Chapter 13 Control of Fat Intake by Striatal Opioids ........................................ 323
Brian A. Baldo, Wayne E. Pratt, and Ann E. Kelley
Chapter 14 Fat-Rich Food Palatability and Appetite Regulation ...................... 345
Charlotte Erlanson-Albertsson
Chapter 15 Fats and Satiety ............................................................................... 375
Rania Abou Samra
Contents ix
PART VI Genetic Factors Influencing Fat
Preference and Metabolism
Chapter 16 Heritable Variation in Fat Preference.............................................. 395
Danielle R. Reed
Chapter 17 Dietary, Physiological, and Genetic Impacts on Postprandial
Lipid Metabolism ............................................................................ 417
José Lopez-Miranda and Carmen Marin
PART VII Lipids and Disease
Chapter 18 Control of Fatty Acid Intake and the Role of Essential Fatty
Acids in Cognitive Function and Neurological Disorders .............. 463
Kiran S. Panickar and Sam J. Bhathena
Chapter 19 What Is the Link between Docosahexaenoic Acid, Cognitive
Impairment, and Alzheimer’s Disease in the Elderly? ................... 485
Michel E. Bégin, Mélanie Plourde, Fabien Pifferi,
and Stephen C. Cunnane
Chapter 20 Hypothalamic Fatty Acid Sensing in the Normal
and Disease States ........................................................................... 507
Madhu Chari, Carol K.L. Lam, and Tony K.T. Lam
Chapter 21 Dietary Fat and Carbohydrate Composition:
Metabolic Disease ........................................................................... 533
Marc A. Brown, Len H. Storlien, Xu-Feng Huang,
Linda C. Tapsell, Paul L. Else, Janine A. Higgins,
and Ian L. Brown
Chapter 22 Food Intake and Obesity: The Case of Fat...................................... 561
Jennifer T. Smilowitz, J. Bruce German,
and Angela M. Zivkovic
Index ...................................................................................................................... 597
Series Preface
Our goal in creating the Frontiers in Neuroscience Series is to present the insights
of experts on emerging fields and theoretical concepts that are, or will be, at the
vanguard of neuroscience. Books in the series cover topics ranging from genetics,
ion channels, apoptosis, electrodes, neural ensemble recordings in behaving animals,
and even robotics. The series also covers new and exciting multidisciplinary areas
of brain research, such as computational neuroscience and neuroengineering, and
describes breakthroughs in classical fields like behavioral neuroscience. We want
these books to be the books every neuroscientist will use in order to get acquainted
with new ideas and frontiers in brain research. These books can be used by graduate
students and postdoctoral fellows when they are looking for guidance to start a new
line of research.
Each book is edited by an expert and consists of chapters written by the leaders
in a particular field. They are richly illustrated and contain comprehensive bibliog-
raphies. All the chapters provide substantial background material relevant to the
particular subject. We hope that as the volumes become available the effort put in
by us, the publisher, the book editors, and individual authors will contribute to the
further development of brain research. The extent that we achieve this goal will be
determined by the utility of these books.
Sidney A. Simon, PhD
Miguel A.L. Nicolelis, MD, PhD
xi
Foreword
Fat—a word that strikes emotions in all of us. Being initially associated with healthy
and nutritious food attributes after World War II the connotation changed toward a
more negative one over the past few decades. It goes without saying that fat—used as
an adjective—for example to describe bodily appearance is close to being politically
incorrect.
At the same time impressive insights accumulated on the role of fat in health and
nutrition. We understand the metabolic breakdown of fat in our bodies as well as
the synthesis and its storage in adipocytes. The role of triglycerides in diabetes and
cardiovascular disease is undisputed and obviously the global obesity epidemic is
firmly linked to food intake and fat.
With the above in mind it is surprising to realize that one aspect of fat never has
been addressed in a comprehensive way—I am talking about the perception, taste,
and smell of dietary fat.
In the present book Fat Detection: Taste, Texture, and Post Ingestive Effects,
edited by Jean-Pierre Montmayeur and Johannes le Coutre, a superb collection of
contributions has been compiled by the pre-eminent authors in the field to address
this topic.
I leave it up to the readers to discover the exciting evolutionary role of fat intake
and to learn how the detection of fat can be monitored from the tongue to the brain
and subsequently how we develop a clear preference for fat—and sometimes also an
aversion.
The important contribution of this book is the demystification of fat from being
the culprit in today’s nutrition toward a positioning of “good fat” as an essential
building block of food to deliver enhanced development and performance as well as
a desirable impact on the prevention of disease.
For the educated amateur scientist with an interest in the principles of sensory
physiology and nutrition the book offers a comprehensible introduction to the field.
For the established expert it provides a balanced overview of the latest developments
in the field.
I am convinced this book will make its contribution toward a more educated but
also toward a more relaxed way of interacting with fat so that we can go to a good
restaurant and consume our fried eggplants, risotto, fish, and dessert knowing that
enjoyable and good food does have a positive impact on our health.
Günter Blobel
John D. Rockefeller, Jr. Professor
Investigator, HHMI Laboratory of Cell Biology
The Rockefeller University, New York
xiii
Preface
The idea to put together a book compiling the current knowledge on dietary fat taste,
perception and intake came about somewhere between a slice of foie gras in Prenois
and a portion of Vacherin cheese in Lausanne during Sid Simon’s visit to Europe in
the spring of 2007. We realized then that the exquisite taste of these foods and hard-
to-resist second helpings might have been related to their fat content.
Why is fat so tasty, why do we crave it, and what is the impact of dietary fat on
health and disease? These are the fundamental questions this book aims to answer
through 22 chapters contributed by leading scientists in the field who deserve all the
credit and all our gratitude for making this project not only possible but most impor-
tantly a very pleasant experience.
The undeniable sensory appeal of fat may have deep roots; some might even argue
that the ability to select energy-dense foods is crucial for survival. Part I of this book
lays down the evolutionary reasons for a fat detection system. In Chapter 1, William
Leonard and colleagues convey archeological arguments linking the availability of
docosahexaenoic acid and diets rich in arachidonic acid with the evolution of larger brain
size in mammals, and in Chapter 2 Frits Muskiet provides an in-depth review of the
importance of dietary fats in development, including geographical and sociocultural
arguments guiding nutritional habits.
Over the last two decades, numerous studies investigating the gustatory mecha-
nisms and sensory factors underlying the innate preference for dietary fat have accu-
mulated. Part II of this book summarizes essential findings emanating from this
significant body of work through five chapters. In Chapter 3, Timothy Gilbertson and
colleagues review the candidate receptor mechanisms underlying oral fat detection
and provide a clear image of the state of the art in fat taste transduction through a
new model piecing together the current players. In Chapter 4, David Pittman high-
lights important findings on the modulation of fatty acids responsiveness by gender
and strain. Next, in Chapter 5 Jennifer Stratford and Robert Contreras lay out behav-
ioral studies that contributed to the mapping of the circuits linking preference and
peripheral detection mechanisms. Then, in Chapter 6 James Smith documents how
carefully designed behavioral paradigms helped establish that gustatory, textural,
and olfactory information all contribute to fat detection. Finally, in a comprehensive
review, in Chapter 7 Richard Mattes reflects on 15 years of psychophysical, behav-
ioral, electrophysiological, and molecular studies, making the case for an oral fat
detection system.
In Part III, Edmund Rolls (Chapter 8) provides a detailed account of the brain
regions processing the signals elicited by a fat stimulus including flavor, aroma, and
texture; their modulation by hunger; and their impact on the pleasantness of food. In
Chapter 9, Ulrike Toepel and colleagues contribute a stimulating chapter on the cor-
tical regions implicated in reward assessment and decision-making, demonstrating
that visual food stimuli initiate a rapid processing of the food’s energetic content.
xv
xvi Preface
There are many explanations for the appeal of fat. Part IV explores some of them
through the contribution of Yasuko Manabe and colleagues (Chapter 10), who review
pioneering behavioral experiments in rodents, and together represent the most com-
pelling evidence that fat is detected in the mouth. In Chapter 11, Adam Drewnowski
and Eva Almiron-Roig accomplish a remarkable feat by covering the many factors
responsible for the sensory appeal of foods rich in fat.
Several of the factors contributing to fat preference, including fat content, palat-
ability, satiety, pleasure, and reward, are discussed in great detail in Part V. First,
Karen Ackroff and Anthony Sclafani (Chapter 12) skillfully summarize key experi-
ments exploring the impact of postoral factors on dietary fat appetite. In Chapter
13, Brian Baldo and colleagues provide a logical and detailed analysis of their find-
ings on the brain mechanisms associated with appetitive behaviors and the hedonic
experience connected with food consumption. Next, Charlotte Erlanson-Albertsson
(Chapter 14) presents an overview of the effect of fatty acids intake on the release of
appetite regulating peptides and makes the case for enterostatin as a potential thera-
peutic target to control fat intake. Finally, Rania Abou Samra (Chapter 15) discusses
the effects of various fats and fatty acids on satiety and appetite as well as those of
other dietary components.
Genetic predisposition and physiological status can influence the intake and
metabolism of fats. In Part VI, Danielle Reed (Chapter 16) addresses the genetic
components of human fat preference with an in-depth look at heritability through
family and twin studies. In Chapter 17, José Lopez-Miranda and Carmen Marin
focus on the impact of lifestyle and the fatty acid composition of meals on postran-
dial lipemia, pointing out a possible link with atherosclerosis.
It has become apparent that there is a link between obesity and the rise in the
consumption of energy-dense diets such as those rich in dietary fats. The first section
of Part VII gathers clinical observations on the link between essential fatty acids and
neurological disorders through the contribution of Kiran Panickar and Sam Bhathena
(Chapter 18) who point out studies suggesting that diets enriched in ω-3 fatty acids
seem to help improve the conditions of Huntington’s disease, stroke, and multiple
sclerosis patients. In addition, Michel Bégin and colleagues (Chapter 19) discuss the
protective value of a seafood diet on cognitive impairment and dementia based on
the results of epidemiological studies. In the remaining chapters of Part VII, Madhu
Chari and colleagues (Chapter 20) present a very thorough account of the current
knowledge on the hypothalamic fatty acid sensing mechanisms as they relate to
energy homeostasis. In Chapter 21, Marc Brown and colleagues review a vast array
of investigations on the contribution of dietary fat and carbohydrates to the devel-
opment of diseases tied to the metabolic syndrome, including detailed molecular
mechanisms underpinning the protective effect of ω-3 polyunsaturated fatty acids
on insulin resistance and obesity. Finally in Chapter 22, Jennifer Smilowitz and col-
leagues investigate the connection between fat metabolism, the fat content of foods,
and obesity, making a loud statement in favor of personalized studies contributing
insights on the impact of diet on the metabolic syndrome.
By gathering information from the many different fields covered, we hope that
this book will not only spark new interests toward this very important topic, but also
Preface xvii
provide a general reference for students, scientists, physicians, and professionals in
the field of food science.
We would like to thank the following people for their help and support through-
out this project: Maia Kokoeva, John Langone, Ronit le Coutre, Anna Montmayeur,
James Stellar, and Gary Strichartz. Most of all we are grateful to Sidney Simon for
extending the invitation to get involved in this series as well as to Jill Jurgensen and
Barbara Norwitz at Taylor & Francis for their patience and efficiency.
A final note: over the course of this project the neuroscience community lost
two distinguished members. Doctors Ann E. Kelley and Sam J. Bhathena are being
remembered with special dedications in Chapters 13 and 18, respectively. We are
indebted to Brian Baldo and Kiran Panickar for kindly accepting to undertake these
chapters on their behalf despite the circumstances.
Jean-Pierre Montmayeur
Johannes le Coutre
