Taste, Olfactory and Food-texture Processing in the Brain and the Control of Appetite

16 Pages·2009·0.39 MB·English

C H A P T E R
4 4
c c00002255 Taste, Olfactory and Food-texture
Processing in the Brain and the Control
of Appetite
Edmund T. Rolls
Oxford Centre for Computational Neuroscience, Oxford, UK
O U T L I N E
4.1 Introduction 42 4.8 Implications for Understanding,
Preventing and Treating Obesity 47
4.2 Taste-Processing in the Primate Brain 42
4.8.1 Brain Processing of the Sensory
4.2.1 Pathways 42
Properties and Pleasantness of Food 49
4.2.2 The Primary Taste Cortex 42
4.8.2 Genetic Factors 49
4.2.3 The Secondary Taste Cortex 42
4.8.3 Endocrine Factors and their
4.2.4 The Pleasantness of the Taste of Food,
Interaction with Brain Systems 50
Sensory-Specific Satiety, and the Effects
4.8.4 Food Palatability 50
of Variety on Food Intake 43
4.8.5 Sensory-specific Satiety and
4.3 The Representation of Flavor:
the Effects of Variety on Food Intake 51
Convergence of Olfactory, Taste and Visual
4.8.6 Fixed Meal-times and the
Inputs in the Orbitofrontal Cortex 44
Availability of Food 51
4.4 The Texture of Food, Including Fat 4.8.7 Food Saliency and Portion Size 51
Texture 44 4.8.8 Energy Density of Food 51
4.5 Imaging Studies in Humans 44 4.8.9 Eating Rate 51
4.5.1 Taste 44 4.8.10 Stress 52
4.5.2 Odor 45 4.8.11 Food Craving 52
4.5.3 Olfactory–taste Convergence to Represent 4.8.12 Energy Output 52
Flavor and the Influence of Satiety 46 4.8.13 Cognitive Factors 52
4.5.4 Oral Viscosity and Fat Texture 46 4.8.14 The Psychology of Compliance with
4.5.5 The Sight of Food 46 Information about Risk Factors
for Obesity 52
4.6 Cognitive Effects on
Representations of Food 46 4.9 Concluding Remarks 52
4.7 Synthesis 47 Acknowledgments 53
41
Obesity Prevention: The Role of Brain and Society on Individual Behavior © 22001100, Elsevier Inc.
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4. FOOD, TASTE, SMELL AND TEXTURE
s s00001100 4.1 INTRODUCTION et al. , 1996a ), but also other neurons that encode
oral somatosensory stimuli, including viscosity,
fat texture, temperature and capsaicin (V erhagen
p p00001100 The aims of this chapter are to describe the
et al. , 2004 ). Some neurons in the primary taste
rules of the cortical processing of taste and
cortex respond to particular combinations of
smell, how the pleasantness or affective value
taste and oral texture stimuli, but do not respond
of taste and smell are represented in the brain,
to olfactory stimuli or visual stimuli (V erhagen
how cognitive factors modulate these affective
et al. , 2004 ). Neurons in the primary taste cortex
representations, and how these affective repre-
do not represent the reward value of taste – that
sentations play an important role in the control
is, the appetite for a food – in that their firing is
of appetite, food intake and obesity. To make the
not decreased to zero by feeding the taste to sati-
results relevant to understanding the control of
ety ( Rolls e t al. , 1988 ; Yaxley et al. , 1988 ).
human food intake, complementary evidence is
provided by neurophysiological studies in non-
human primates, and by functional neuroimag-
s s00003300 ing studies in humans. A broad perspective of 4.2.3 The secondary taste cortex
the brain processing involved in emotion and in
p p00002255 A secondary cortical taste area in primates
hedonic aspects of the control of food intake is
was discovered by Rolls, Yaxley and Sienkiewicz
provided by R olls (2005a) .
in the caudolateral orbitofrontal cortex, extend-
ing several millimeters in front of the primary
taste cortex (R olls e t al. , 1990 ). Neurons in this
s s00001155 4.2 TASTE-PROCESSING IN THE
region respond not only to each of the four clas-
PRIMATE BRAIN
sical prototypical tastes sweet, salt, bitter and
sour (R olls, 1997; Rolls and Scott, 2003 ); many
also respond best to umami tastants such as
4.2.1 Pathways s s00002200
glutamate (which is present in many natural
A diagram of the taste and related olfactory, foods, such as tomatoes, mushrooms and milk) p p00001155
somatosensory and visual pathways in primates ( Baylis and Rolls, 1991 ), and inosine monophos-
is shown in F igure 4.1 . The multimodal conver- phate (which is present in meat and some fish,
gence that enables single neurons to respond to such as tuna) (R olls e t al. , 1996a ). This evidence,
different combinations of taste, olfactory, tex- taken together with the identification of gluta-
ture, temperature and visual inputs to represent mate taste receptors ( Zhao e t al. , 2003 ; Maruyama
different flavors produced by often new com- et al. , 2006 ), leads to the view that there are five
binations of sensory inputs is a theme of recent prototypical types of taste information channels,
research that will be described. with umami contributing, often in combination
with corresponding olfactory inputs (R olls et al. ,
1998 ; McCabe and Rolls, 2007 ; Rolls, 2009) , to
the flavor of protein. In addition, other neurons
s s00002255 4.2.2 The primary taste cortex
respond to water and some to somatosensory
p p00002200 The primary taste cortex in the primate anterior stimuli, including astringency as exemplified by
insula and adjoining frontal operculum contains tannic acid (C ritchley and Rolls, 1996a) , and cap-
not only taste neurons tuned to sweet, salt, bitter, saicin (R olls e t al. , 2003a ; Kadohisa et al. , 2004 ).
sour ( Scott et al. , 1986 ; Yaxley et al. , 1990 ; Rolls and Taste responses are found in a large mediolateral
Scott, 2003) and umami as exemplified by mono- extent of the orbitofrontal cortex (P ritchard e t al. ,
sodium glutamate (B aylis and Rolls, 1991; Rolls 2005 ; Rolls, 2008 ; Rolls and Grabenhorst, 2008) .
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4.2 TASTE-PROCESSING IN THE PRIMATE BRAIN
VISION
Inferior temporal
V1 V2 V4
visual cortex
Cingulate cortex
Behavior
Amygdala Striatum
Behavior
TASTE
Taste Nucleus of the Thalamus Lateral
receptors solitary tract VPMpc nucleus hypothalamus
Autonomic
Gate Gate responses
Frontal operculum/Insula function
(Primary taste cortex) Orbitofrontal
cortex
Hunger neuron controlled
by e.g. glucose utilization,
stomach distension or body
weight
OLFACTION
Olfactory Olfactory (Pyriform)
Bulb cortex
Insula
TOUCH
Thalamus VPL Primary somatosensory cortex (1.2.3)
f f00001100 FIGURE 4.1 Schematic diagram of the taste and olfactory pathways in primates including humans showing how they
converge with each other and with visual pathways.
Hunger modulates the responsiveness of the representations in the orbitofrontal cortex of the taste, smell, texture and sight
of food (indicated by the gate function), and the orbitofrontal cortex is where the palatability and pleasantness of food is
represented.
VPMpc, ventralposteromedial thalamic nucleus; V1, V2, V4, visual cortical areas.
4.2.4 The pleasantness of the taste of correlate of this modulation is that food tastes s s00003355
food, sensory-specific satiety, and the pleasant when hungry, and tastes hedonically
neutral when it has been eaten to satiety. The dis-
effects of variety on food intake
covery of sensory-specific satiety was revealed
The modulation of the reward value of a sen- by the selective reduction in the responses of p p00003300
sory stimulus such as the taste of food by moti- lateral hypothalamic neurons to a food eaten to
vational state – for example, hunger – is one satiety (R olls, 1981; R olls e t al. , 1986 ). It has been
important way in which motivational behavior shown that this is implemented in a region that
is controlled ( Rolls, 2005a, 2007) . The subjective projects to the hypothalamus, the orbitofrontal
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4. FOOD, TASTE, SMELL AND TEXTURE
cortex (secondary taste), for the taste, odor, sight of the food, as shown by sensory-specific satiety
and texture of food (R olls et al. , 1989 ; Critchley effects (C ritchley and Rolls, 1996b ).
and Rolls, 1996b; Rolls et al. , 1999 ).
This evidence shows that the reduced accept- p p00003355
ance of food that occurs when food is eaten to 4.4 THE TEXTURE OF FOOD, s s00004455
satiety, the reduction in the pleasantness of its INCLUDING FAT TEXTURE
taste and flavor, and the effects of variety to
increase food intake ( Cabanac, 1971; Rolls and
Some orbitofrontal cortex neurons have oral p p00004455
Rolls, 1977, 1982, 1997 ; Rolls et al. , 1981a, 1981b,
texture-related responses that encode para-
1982, 1983a, 1983b, 1984 ; Rolls and Hetherington,
metrically the viscosity of food in the mouth
1989 ; Hetherington, 2007) are produced in the
(shown using a methyl cellulose series in the
orbitofrontal cortex, but not at earlier stages of
range 1– 10,000 centiPoise). Others independ-
processing where the responses reflect factors
ently encode the particulate quality of food in
such as the intensity of the taste, which is little
the mouth, produced quantitatively, for exam-
affected by satiety ( Rolls et al. , 1983c ; Rolls and
ple, by adding 20- to 100- μ m microspheres to
Grabenhorst, 2008) . In addition to providing
methyl cellulose (R olls e t al. , 2003a ). Others,
an implementation of sensory-specific satiety
finally, encode the oral texture of fat ( Rolls
(probably by habituation of the synaptic affer-
et al. , 1999 ; Verhagen et al. , 2003 ), as illustrated
ents to orbitofrontal neurons with a time-course
in F igure 4.2 . In addition, some neurons in the
of the order of length of a meal course), it is
orbitofrontal cortex reflect the temperature of
likely that visceral and other satiety-related sig-
substances in the mouth ( K adohisa et al. , 2004,
nals reach the orbitofrontal cortex (as indicated
2005 ). This temperature information is repre-
in Figure 4.1 ) (from the nucleus of the solitary
sented independently of other sensory inputs
tract, via thalamic and possibly hypothalamic
by some neurons, and in combination with taste
nuclei), and there modulate the representation
or texture by other neurons.
of food, resulting in an output that reflects the
reward (or appetitive) value of each food (R olls,
2005a ).
s s00005500 4.5 IMAGING STUDIES IN
HUMANS
s s00004400 4.3 THE REPRESENTATION OF
FLAVOR: CONVERGENCE OF
s s00005555 4.5.1 Taste
OLFACTORY, TASTE AND VISUAL
p p00005500 INPUTS IN THE ORBITOFRONTAL In humans, it has been shown in neuroimag-
ing studies using functional magnetic resonance
CORTEX
imaging (fMRI) that taste activates an area of
the anterior insula/frontal operculum, which
p p00004400 Taste and olfactory pathways are brought is probably the primary taste cortex, and part
together in the orbitofrontal cortex, where flavor of the orbitofrontal cortex, which is probably
is formed by learned associations at the neuronal the secondary taste cortex (F rancis et al. , 1999 ;
level between these inputs (see F igure 4.1 ) ( Thorpe O’Doherty e t al. , 2001 ; de Araujo et al. , 2003a ).
et al. , 1983 ; Rolls and Baylis, 1994 ; Critchley Within individual subjects, separate areas of the
and Rolls, 1996c; Rolls, 1996 ; Rolls et al. , 1996b ; orbitofrontal cortex are activated by sweet (pleas-
Verhagen e t al. , 2004) . The visual and olfactory as ant) and by salt (unpleasant) tastes (O ’Doherty
well as the taste inputs represent the reward value et al. , 2001 ).
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4.5 IMAGING STUDIES IN HUMANS
Fat responsive neurons respond independently of viscosity e.g.
20
bk265
ec; 15
es/sm) vegetable oil 55
pikse safflower oil 50
ate (san+/– 10 mineral oil 25 280 silicone oil
Firing rme 5 40 coconut oil
CMC series
0
1 10 100 1000 10,000
Viscosity (cP)
f f00001155 FIGURE 4.2 A neuron in the primate orbitofrontal cortex responding to the texture of fat in the mouth independently of
viscosity.
The cell (bk265) increased its firing rate to a range of fats and oils (the viscosity of which is shown in centiPoise). The information
that reaches this type of neuron is independent of a viscosity-sensing channel, in that the neuron did not respond to the methyl
cellulose (CMC) viscosity series. The neuron responded to the texture rather than the chemical structure of the fat in that it also
responded to silicone oil (Si(CH3)2O)n) and paraffin (mineral) oil (hydrocarbon). Some of these neurons have taste inputs.
Source : Adapted from Verhagen and colleagues (2003).
p p00005555 We also found activation of the human amy- ( Rolls, 2009 ). Overall, these results illustrate that
gdala by the taste of glucose (F rancis e t al. , 1999 ). the responses of the brain can reflect inputs pro-
Extending this study, O’Doherty and colleagues duced by particular combinations of sens ory
(2001) showed that the human amygdala was as stimuli with supralinear activations. The combi-
much activated by the affectively pleasant taste nation of sensory stimuli may be especially rep-
of glucose as by the affectively negative taste of resented in particular brain regions, and may
salt, and thus provided evidence that the human help to make the food pleasant.
amygdala is not especially involved in processing
aversive as compared to rewarding stimuli. Zald
4.5.2 Odor s s00006600
and colleagues (1998) had shown earlier that the
amygdala, as well as the orbitofrontal cortex, In humans, in addition to activation of the p p00006655
responds to aversive (saline) taste stimuli. pyriform (olfactory) cortex (Z ald and Pardo, 1997 ;
p p00006600 Umami taste stimuli activate the insular Sobel et al. , 2000 ; Poellinger et al. , 2001 ), there is
(primary), orbitofrontal (secondary) and ante- strong and consistent activation of the orbitof-
rior cing ulate (tertiary; R olls, 2008) taste cor- rontal cortex by olfactory stimuli (Z atorre et al. ,
tical areas ( de Araujo et al. , 2003b ). When the 1992 ; Francis et al. , 1999 ). This region appears
nucleotide 0.005-M inosine 5(cid:2) -monophosphate to represent the pleasantness of odor, as shown
(IMP) was added to MSG (0.05 M), the BOLD by a sensory-specific satiety experiment with
(blood oxygenation-level dependent) signal in banana versus vanilla odor (O ’Doherty e t al. ,
an anterior part of the orbitofrontal cortex sho- 2000 ). Further, pleasant odors tend to activate the
wed suprali near additivity. This may reflect the medial, and unpleasant odors the more lateral,
subjective enhancement of umami taste that orbitofrontal cortex ( Rolls e t al. , 2003b ), adding
has been desc ribed when IMP is added to MSG to the evidence that there is a hedonic map in the
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4. FOOD, TASTE, SMELL AND TEXTURE
s s00007700 orbitofrontal cortex and in the anterior cingulate 4.5.4 Oral viscosity and fat texture
cortex, which receives inputs from the orbitofron-
p p00008855 The viscosity of food in the mouth is repre-
tal cortex (R olls and Grabenhorst, 2008) .
sented in the human primary taste cortex (in the
anterior insula), and also in a mid-insular area that
is not taste cortex but which represents oral som-
4 .5.3 Olfactory – taste convergence to s s00006655
atosensory stimuli (d e Araujo and Rolls, 2004) .
represent flavor and the influence of satiety
Oral viscosity is also represented in the human
orbitofrontal and perigenual cingulate cortices. It
Supra -additive effects indicating conver- p p00007700
is notable that the pregenual cingulate cortex, an
gence and interactions were found for taste
area in which many pleasant stimuli are repre-
(sucrose) and odor (strawberry) in the orbitof-
sented, is strongly activated by the texture of fat
rontal and anterior cingulate cortex. Activations
in the mouth and by oral sucrose ( de Araujo and
in these regions were correlated with the pleas-
Rolls, 2004) . The pleasantness of fat texture may
antness ratings given by the participants (d e
be represented in the orbitofrontal and anterior
Araujo e t al. , 2003c ; Small et al. , 2004 ; Small and
cingulate cortex, for activations in these regions
Prescott, 2005 ). These results provide evidence
are correlated with the subjective pleasantness of
on the neural substrate for the convergence of
fat ( Grabenhorst e t al. , 2009 ).
taste and olfactory stimuli to produce flavor in
humans, and on where the pleasantness of fla- s s00007755
vor is represented in the human brain.
4.5.5 The sight of food
M cCabe and Rolls (2007) have shown that the p p00007755
convergence of taste and olfactory information
O ’Doherty and colleagues (2002) showed p p00009900
appears to be important for the pleasantness of
that visual stimuli associated with the taste of
umami. They showed that when glutamate is
glucose activated the orbitofrontal cortex and
given in combination with a consonant savory
some connected areas, consistent with the pri-
odor (vegetable), the resulting flavor can be much
mate neurophysiology. Simmons, Martin and
more pleasant than the glutamate taste or vege-
Barsalou found that showing pictures of foods,
table odor alone. This reflected activations in
compared to pictures of locations, can also acti-
the pregenual cingulate cortex and medial orbit-
vate the orbitofrontal cortex ( Simmons e t al. ,
ofrontal cortex. Certain sensory combinations,
2005 ). Similarly, the orbitofrontal cortex and
therefore, can produce very pleasant food stimuli,
connected areas were also found to be acti-
which may be important in driving food intake.
vated after presentation of food stimuli to food-
p p00008800 To assess how satiety influences the brain acti-
deprived subjects (W ang et al. , 2004 ).
vations to a whole food which produces taste,
olfactory and texture stimulation, we measured
brain activation by whole foods before and after 4.6 COGNITIVE EFFECTS ON s s00008800
the food is eaten to satiety ( de Araujo et al. , 2003b ).
REPRESENTATIONS OF FOOD
The foods eaten to satiety were either chocolate
milk or tomato juice. A decrease in activation by
the food eaten to satiety relative to the other food To what extent does cognition influence the p p00009955
was found in the orbitofrontal cortex ( Kringelbach hedonics of food-related stimuli, and how far
et al. , 2003 ) but not in the primary taste cortex. down into the sensory system does cognitive
This study provided evidence that the pleasant- influence reach? To address this, we performed
ness of the flavor of food and sensory-specific an fMRI investigation in which the delivery of a
satiety are represented in the orbitofrontal cortex. standard test odor (isovaleric acid combined with
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4.8 IMPLICATIONS FOR UNDERSTANDING, PREVENTING AND TREATING OBESITY
Cheddar cheese flavor, presented orthonasally to the hypothalamus, where neurons are found
using an olfactometer) was paired with a descrip- that respond to the sight, smell and taste of
tor word on a screen, which on different trials was food if hunger is present ( Rolls, 2007 ; Rolls and
“ Cheddar Cheese” or “ Body Odor ” . Participants Grabenhorst, 2008) . We have seen above some of
rated the affective value of the test odor as sign i- the principles that help to make the food pleas-
ficantly more pleasant when labeled “ Cheddar ant, including particular combinations of taste,
Cheese ” than when labeled “ Body Odor ” . These olfactory, texture, visual and cognitive inputs.
effects reflected activations in the medial orbit- Below is developed a hypothesis that obesity is
ofrontal cortex (OFC)/rostral anterior cingu- associated with overstimulation of these reward
late cortex (ACC) that had correlations with the systems by very rewarding combinations of
pleasantness ratings (d e Araujo et al. , 2005 ) (see taste, odor, texture, visual and cognitive inputs.
Figure 4.3 ).
The implication is that cognitive factors can p p00110000
have profound effects on our responses to the 4.8 IMPLICATIONS FOR s s00009900
hedonic and sensory properties of food: these UNDERSTANDING, PREVENTING
effects are manifest quite far down into sen-
AND TREATING OBESITY
sory processing, so that hedonic representations
of odors are affected (de Araujos et al. , 2005).
Similar cognitive effects and mechanisms have Understanding the mechanisms that control p p00111100
now been found for the taste and flavor of food appetite is becoming an increasingly important
( Grabenhorst e t al. , 2008 ). In addition, it has been issue, given the growing incidence of obesity
found that with taste, flavor and olfactory food- (a three-fold increase in the UK since 1980 to a
related stimuli, attention to pleasantness modu- figure of 20 percent, as defined by a BMI (cid:3) 30)
lates representations in the orbitofrontal cortex, and its association with major health risks (with
whereas attention to intensity modulates activa- 1000 deaths each week in the UK attributable
tions in areas such as the primary taste cortex to obesity). It is important to understand and
( Grabenhorst and Rolls, 2008; Rolls e t al. , 2008 ). thereby be able to minimize and treat obesity,
because many diseases are associated with a
body weight that is much above normal. These
diseases include diabetes, hypertension, cardi-
s s00008855 4.7 SYNTHESIS
ovascular disease, hypercholesterolaemia and
gall bladder disease; in addition, obesity is ass-
p p00110055 These investigations show that representations o ciated with some deficits in reproductive
of the reward/hedonic value and pleasantness function (e.g., ovulatory failure) and an excess
of sensory, including food-related, stimuli in the mortality from certain types of cancer (G arrow,
brain are formed separately from representations 1988 ; Barsh and Schwartz, 2002 ; C ummings
of what the stimuli are. The pleasantness/reward and Schwartz, 2003 ; Schwartz and Porte, 2005 ).
value is represented in areas such as the orbitof- There are many factors that can cause or con-
rontal cortex and pregenual cingulate cortex. It is tribute to obesity in humans (B rownell and
here that satiety signals modulate the representa- Fairburn, 1995 ; Morton et al. , 2006 ; O’Rahilly
tions of food to make them implement reward so and Farooqi, 2006 ) that are investigated with
that they only occur when hunger is present. The approaches within or related to neuroscience
satiety signals that help in this modulation may and psychology ( R olls, 2005a, 2005b, 2006,
reach the orbitofrontal cortex from the hypotha- 2007 ). Rapid progress is being made in under-
lamus. In turn, the orbitofrontal cortex projects standing these, with the aim of leading to better
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4. FOOD, TASTE, SMELL AND TEXTURE
a b
R
X=13 Y=42
z
0 2 4
c d
Y=0 Y=15
e f
0.7
0.4
e) 0.5
g
n
0.0 ha
%c 0.2
D (
L
O 0
–0.4 B
16 2 16 2
8 0 1 1
–1 8 0
PST (sec) 0–2 Pleasantness PST (sec) –1 Pleasantness
0
ratings –2 ratings
f f00002200 FIGURE 4.3 C ognitive influences on olfactory representations in the human brain.
Group (random) effects analysis showing the brain regions where the BOLD signal was correlated with pleasantness rat-
ings given to the test odor. The pleasantness ratings were being modulated by the word labels. (a) Activations in the rostral
anterior cingulate cortex, in the region adjoining the medial OFC, shown in a sagittal slice. (b) The same activation shown
coronally. (c) Bilateral activations in the amygdala. (d) These activations extended anteriorly to the primary olfactory cortex.
The image was thresheld at P (cid:4) 0.0001 uncorrected in order to show the extent of the activation. (e) Parametric plots of the
data averaged across all subjects showing that the percentage BOLD change (fitted) correlates with the pleasantness ratings
in the region shown in (a) and (b). The parametric plots were very similar for the primary olfactory region shown in D. PST,
post-stimulus time(s). (f) Parametric plots for the amygdala region shown in (c).
Source : Adapted from DeAraujo e t al ., 2005.
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4.8 IMPLICATIONS FOR UNDERSTANDING, PREVENTING AND TREATING OBESITY
ways to minimize and treat obesity. These fac- food and how the system is modulated by eat-
tors include the following: ing and satiety. This understanding, and how
the sensory factors can be designed and con-
trolled so as not to override satiety signals, are
4.8.1 Brain processing of the sensory important research areas in the understanding, s s00009955
properties and pleasantness of food prevention and treatment of obesity. Advances
in understanding the receptors that encode the
The way in which the sensory factors pro- taste and olfactory properties of food (B uck, p p00111155
duced by the taste, smell, texture and sight of 2000 ; Zhao et al. , 2003 ), and the processing in
food interact in the brain with satiety signals the brain of these properties ( Rolls, 2004, 2005a,
(such as gastric distension and satiety-related 2005b ), are also important in providing the
hormones) to determine the pleasantness and potential to produce highly palatable food that
palatability of food, and therefore whether is at the same time nutritious and healthy.
p p00113300 and how much food will be eaten, is described An important aspect of this hypothesis is that
above and shown in Figures 4.1 and 4.4 . The different humans may have reward systems that
concept is that convergence of sensory inputs are strongly driven by the sensory and cognitive
occurs in the orbitofrontal cortex and builds a factors that make food highly palatable. In a test
representation of food flavor. The orbitofron- of this, we showed that activation to the sight
tal cortex is where the pleasantness and palat- and flavor of chocolate in the orbitofrontal and
ability of food are represented, as demonstrated pregenual cingulate cortex was much higher in
by the discoveries that these representations chocolate cravers and non-cravers (R olls and
of food are only activated if hunger is present, McCabe, 2007 ). The concept that individual dif-
and correlate with the subjective pleasantness ferences in responsiveness to food reward are
of the food flavor ( R olls, 2005a, 2005b, 2006, reflected in brain activations in regions related
2007 ; Rolls and Grabenhorst, 2008 ) The orbitof- to the control food intake ( Beaver et al. , 2006 ;
rontal cortex representation of whether food is Rolls and McCabe, 2007 ; Lowe et al. , 2009 ; Van
pleasant (given any satiety signals present) then den Eynde and Treasure, 2009 ) may provide a
drives brain areas such as the striatum and cin- way for understanding and helping to control
gulate cortex that then lead to eating behavior. food intake.
p p00112200 In the context of the obesity crisis, the past 30
years have seen a dramatic increase of the sensory
stimulation produced by the taste, smell, texture
s s00110000 4.8.2 Genetic factors
and appearance of food, as well as its availabil-
p p00113355 ity. Conversely, the satiety signals produced by Genetic factors are of some importance, with
stomach distension, satiety hormones, etc., have some of the variance in weight and resting met-
remained essentially unchanged. The effect on abolic rate in a population of humans attributa-
the brain’s control system for appetite (shown ble to inheritance (M orton et al. , 2006 ; O’Rahilly
in Figures 4.1 and 4.4 ) is to lead to a net average and Farooqi, 2006, 2008 ). However the “ obesity
increase in the reward value and palatability of epidemic” that has occurred since the 1990s can-
food which overrides the satiety signals, con- not be solely attributed to genetic changes, for
tributes to the tendency to be over-stimulated by which the timescale is far too short. Factors such
food, and therefore leads to overeating. as the increased palatability, variety and avail-
In this scenario, it is important to better ability of food (as well as less exercise), crucial p p00112255
understand the rules used by the brain to pro- drivers of food intake, and the amount of food
duce the representation of the pleasantness of that is eaten ( R olls, 2005a, 2005b, 2006, 2007) are
1. FROM BRAIN TO BEHAVIOR
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50
4. FOOD, TASTE, SMELL AND TEXTURE
Obesity: sensory factors that make food increasing palatable
may over-ride existing satiety signals
Cognitive factors:
Conscious rational control
Beliefs about the food
Advertising
Sensory factors:
Taste
Smell
Texture
Sight Brain mechanisms:
Eating,
Sensory factors modulated
autonomic,
by satiety signals
Effects of: and endocrine
produce reward value
Variety effects
and appetite
Sensory-specific satiety
Palatability
Food concentration
Portion size
Ready availability
Satiety / hunger signals:
Adipose signals
Gut hormones
Gastric distension
f f00002255 FIGURE 4.4 O besity: sensory factors that make food increasingly palatable may over-ride existing satiety signals.
Schematic diagram to show how sensory factors interact in the orbitofrontal cortex with satiety signals to produce the hedonic,
rewarding value of food, which leads to appetite and eating. Cognitive factors directly modulate this system in the brain.
more likely to be responsible for the upsurge in 2006 ; Farooqi and O’Rahilly, 2009 ). Further,
the incident of obesity. obese people generally have high levels of lep-
tin, so leptin production is not the problem.
Instead, leptin resistance (i.e., insensitivity) may
4.8.3 Endocrine factors and their be somewhat related to obesity, with the resist- s s00110055
ance perhaps related in part to smaller effects of
interaction with brain systems
leptin on arcuate nucleus NPY/AGRP neurons
A small proportion of cases of obesity can ( Munzberg and Myers, 2005 ). p p00114400
be related to gene-related dysfunctions of the
peptide systems in the hypothalamus, with, for
example, 4 percent of obese people having defi-
4.8.4 Food palatability s s00111100
cient (MC4) receptors for melanocyte stimu-
lating hormone (M orton e t al. , 2006 ; O’Rahilly A factor in obesity is food palatability, which, p p00114455
and Farooqi, 2006 ). Cases of obesity that can be with modern methods of food production, can
related to changes in the leptin hormone satiety now be greater than would have been the case dur-
system are very rare ( O’Rahilly and Farooqi, ing the evolution of our feeding control systems.
1. FROM BRAIN TO BEHAVIOR
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