Olfactory and taste sensory-specific satiety

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Specific hungers & specific appetites

There is also the qualitative regulation of nutrient choice, destined to compensate for protein and ionic deficiency which leads a deprived animal to choose foods that will compensate for the specific deficiency. However, qualitative regulation has only partially been evidenced in man [2].
The deficiency of specific anabolic nutrients like minerals or vitamins in the internal milieu must be corrected by increasing intake of the particular substance. While the specific hunger mechanisms that ensure increased intake still need to be elucidated, there is some evidence in animals that nutrient deficiency causes a specific rise in responsiveness to food containing the substance needed [82].
Much pioneering work in this field was done in the 1940s by Curt Paul Richter and E.M. Scott who originally were the first to use the term ‘specific hungers’ which was later replaced by ‘specific appetites’.
Specific deficiencies are implicated in growth failure [83]. Therefore it seems likely that during evolution, species have evolved to develop chemosensory systems that detect 1, deficiency of crucial elements within their internal milieu, and 2, the presence of that element capable of correcting this deficiency within their external environment. In this way, taste was found to play a crucial role in recovery from specific nutrient deficiencies in rats [84] and postingestive feedback has been identified as a major determinant of food preference in ruminants [85]. Similarly, in accordance with the ‘self-selection method’ food choice adapted to nutritional needs has been observed in neonates [334], children [86,87] and adults [335].
However, it is not entirely clear how a mammalian organism is able to integrate the multitude of specific needs (macronutrients, specific amino-acids, fatty acids, vitamins, salts, oligo-elements etc.) into specific appetites in order to avoid deficiency in any of these vital elements and to what extent the chemical senses are implicated in the genesis of specific appetites.

Alimentary alliesthesia (AA)

The pleasure derived from sweet and salty taste is reduced by the respective presence of carbohydrates and salt in the small intestine and does not require stimulation of the chemical senses. It was suggested that the origin of gustatory alliesthesia (cf chapter on alliesthesia) for sweet taste lies in the duodeno-jejunal vagal glucoreceptors discovered by Mei [240,136,137], which convey afferent sensory information to the CNS.

Sensory-specific satiety (SSS)

The reward-value of a food eaten diminishes gradually during intake, but leaves other foods with distinct sensory properties, present but not eaten in the same meal relatively unaffected, a fact which was confirmed by objective brain imaging techniques in primates and humans. (cf chapter on sensory-specific satiety)

Integration of signals

It has been stated that because of the delay between the swallowing of food and the digestion of food, the satiety mechanism requires a short-term signal to prevent over-eating. That short-term satiety signal might be induced by hedonic functions like SSS, chemical senses and mechanical feedback related to swallowing and gastric distension [374].
However, despite all the efforts into the study of peripheral and central mechanisms of ingestive behavior in thousands of publications on the anatomy, chemistry and metabolism, physiology and behavioral aspects of feeding, we will lack an understanding of the interactions among signals of different systems [374].

Environmental and behavioral factors

The physiological regulation of food intake can be modulated by psychological, social and environmental factors which can disrupt its balance, in part explaining the frequency of over- and underweight [2].
Prior experience, as well as educational, family or social conditioning can have an important impact on food-related behavior, by reinforcing or by antagonizing signals related to energy status.

Social, cultural and environmental factors

In humans, social, cultural and family rules condition food intake behavior from early childhood. They intervene by determining the norms and schedule of food intake.
1. Portion size and caloric compensation: Both, the effects of portion size and of the bottomless bowl (a soup bowl that was constantly and secretly refilled by a tube from underneath) were described by Brian Wansink [138,139,140]. Psycho-behavioral conditioning can override sensory control of food intake, especially in children. Children tend to eat what they are served, meal size thus predicts and dictates calories ingested. In an experiment, children did not adjust their intake to the energy density of the meal or to the energy consumed as snacks between meals, indicating that, similar to adults, they display very poor regulation of energy intake and are more responsive to environmental stimuli [141].
Similarly in young adults (undergraduate students) when given access to a buffet, the amount consumed increased with serving sizes [142].
Unlike rats, following an imposed period of overfeeding, young adults did not reduce their mean daily caloric intake to return to their baseline weight before overfeeding [143].
When humans are challenged with overfeeding, underfeeding, or changes in the caloric density of the diet, they fail to demonstrate precise caloric compensation. However, humans appear to be very sensitive to changes in environmental stimuli [144].
2. Ambiance & distractors: The cultural perception of ideal body-shape can influence food intake behavior. Also environmental stimuli like ambient temperature, light, noise, or complex influences like eating in a restaurant and the number of ‘co-eaters’ influence food intake [145].
3. Physical activity: Importantly, a rise in energy intake does not increase body fat mass if this is accompanied by an equivalent increase in energy expenditure through physical exercise. However, if energy intake exceeds expenditure, this results in a positive energy balance. As an example, Americans have gradually been increasing their mean energy intake since 1970, while their self-reported physical activity remained constant, at least during the 1990s [146].

Psycho-affective factors

Psycho-affective factors (like mood, emotions, anxiety, psychological stress…) can influence food intake, especially in women [147]. In particular, these factors can interact with food-related sensory cues (aspect, odor, taste of food). Thus, ‘reinterpretation’ of sensory information by limbic structures and the cerebral cortex allows confrontation with former experience, mood, or emotional state. Thereby, sensory signals can take an emotional dimension and arouse feelings which influence food intake, i.e., anticipated pleasure, desire, culpability, frustration, or disgust.
This can lead to extremes like disinhibition (i.e., the mental loss of control over food intake) on the one hand, or dietary restraint (i.e., refusal of caloric intake), on the other [148].
Whenever food sensory pleasure is uncoupled from usefulness for the individual (because it is associated with negative sensations of unwanted weight gain), affective factors can override internal needs and can manifest themselves as eating disorders, responsible for sometimes serious weight anomalies.

Cognitive factors

Even though food intake-related behavior is basically motivated by internal energy needs and metabolic substrates, it remains voluntary behavior, which depends on the conscious decision of the individual. Thus, if internal needs lead to a feeling of hunger and a high level of motivation with respect to food intake, the individual preserves the voluntary capacity not to consume food. For example, in certain particular situations, urgent behavior has priority (escape of danger, following of a social or professional obligation…) can be privileged and can suppress or delay food intake. The will to lose weight can also lead to the voluntary restriction of food intake. In this cognitive restriction, it is no longer feelings of hunger and satiety that determine food intake, but the conscious decision of being authorized or prohibited to eat.

Aggregate state of foods

The physical state (solid versus liquid) and the texture (hard versus soft) may influence appetite control and metabolism. The consistency of foods determines the amount of chewing necessary to grind and swallow, which in turn produces feedback from sensory stimulation. Therefore, harder foods produce more sensory satiation than softer ones.
In line with this, two studies [323,324] suggested that fluid calories from beverages are not completely taken into account by the CNS. Another study observed that calories ingested in a liquid form are not well taken in account and could induce a subsequent overconsumption, at least until satiety was conditioned to the fluid [155].
However, this observation has been challenged, in that very few longitudinal cohort studies have investigated soft drink consumption and body weight change [156].
Further, the physical state also determines the duration of gastrointestinal passage. Fluids pass through the stomach quickly and thus do not create a lot of gastric distension. Also, energy rich soft-drinks or alcoholic beverages did not exist in the environment in which humans evolved. The main beverage was non-caloric water, which has have been the main source of fluid intake until very recently in human history, while coconut milk or palm sap depend on regional availability. In addition, (caloric) fruit juices have been available only very recently on a phylogenetic timescale as they require a series techniques (for extraction) and inventions (recipients; selection of juicier fruit varieties – wild fruit is more fibrous than today’s hybrids). It is thus unlikely that the primate satiation mechanisms have been selected to readily detect calories in fluids.

Organoleptic properties of food

While non-human primates and other mammalian species eat food “as is”, i.e. without any processing, humans have learned to modify their foods before intake. Refinement, i.e. food processing (grinding, extraction, thermal denaturation) may affect food intake in several ways: On the one hand, it generally leads to nutrient- and thus energy-concentration. On the other hand, heating foods creates new chemical species like Maillard molecules [157], aromatic substances which are known to enhance the organoleptic properties of foods [158,159,160]. In this way, mixing and seasoning of foods can suppress the astringent properties of foods and thus contribute to increased intake (as will be demonstrated in the first study of this thesis [425]. Finally, the more refined a food is, the less fiber it will contain, fiber which are known to expand in the intestines by water uptake.

Physical aggressions

Exteroceptive physical stress (i.e. painful stimuli or unpleasant sensory stimuli of external origin, e.g. a very noisy environment) can influence food intake. The mechanisms brought into play are only partially characterized. Generally, they implicate conscious psycho-affective and cognitive processes.
Enteroceptive physical stress (which corresponds to aggressions having consequences on the ‘internal milieu’) can also modulate food intake. Bacterial or viral infections or other diseases like cancers or inflammatory syndromes are connected with enteroceptive stress. These diseases influence (generally reduce) food intake via cytokines and other mediators of inflammation which act at the level of the central nervous system.

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Visualization and frequency of specific behaviors

In animals, classically rats, the subject is prepared with both, oral and naso-gastric or naso-duodenal tubes, in order to give bursts of taste samples of defined volume, concentration and at defined moments in time. In contrast to human subjects, who spit out the sample after evaluation, rats swallow it. The ‘hedonic note’, as animals are unable to communicate to the observer what they perceive, is interpreted from the characteristic behavioral response-sequence following the oral load, the occurrence of which is counted. Berridge, Grill and Norgren found out that facial expressions of rats tasting sweet and bitter solutions corresponded to positive and negative hedonic sensations, reflecting pleasure and disgust just as in human subjects [216,217,218,219,220,221]. Hedonically positive reactions (Figures 6 and 7), called ‘ingestive facial consummatory responses’ (i.e. paw licking, lateral tongue protrusions, midline tongue protrusions, mouth movements, passive drip) are differentiated from hedonically negative ones (Figures 8 and 9), called ‘aversive facial consummatory responses’ (i.e. gapes, chin rubs, face washing, forelimb flailing, headshakes, locomotion) [254,255,257,256]. The facial expressions and specific postures of the rat, which is sitting in a transparent cage, are recorded by direct observation or via video camera (Figure 10) and subsequently frame-by-frame analyzed for quantification of the frequency of occurrence of hedonic signals.

Visual and auditory alliesthesia – Environmental alliesthesia

Alliesthesia even extends to the visual modality [263]: the pleasantness of a given color has been described to be a function of circadian rhythm, i.e. from day- to nighttime. Although less evident, it does exist. Daytime exposure to bright or dim light influences color preference in the evening. ‘Warmer’ colors are preferred after dim exposure, due to a higher set-point of core temperature after dim light. After bright light exposure, core temperature is lower and skin temperature higher during sleep [263].
Visual and auditory modalities (i.e. environmental conditions) are subject to alliesthesia. Actually, strong visual and auditory stimulations become more and more pleasant during the day in a state of vigilance while they become more and more unpleasant in a state of fatigue and vice versa [275]. The state of vigilance and fatigue may correspond to a change in the internal milieu.

Alliesthesia for sexual cues

Sexual exhaustion in male rats has been proposed as a case of alliesthesia. For the individual engaged in sexual behavior, its only purpose is its execution. Repeated execution of copulatory acts may reduce the reward value of the female or of the execution of copulatory reflexes. In the absence of sexual consummatory behavior, negative alliesthesia diminishes over time.
On the other hand, the Coolidge effect [345], a phenomenon in which males show renewed sexual interest in a novel female following copulation to satiety with another female, could be an example of dishabituation or could be related to negative sexual alliesthesia. However, these interpretations are based on behavioral observations. Measurements of hedonic correlates would be necessary to confirm or rule out the hypothesis that sexual behavior is in fact a case of alliesthesia. Also human studies support these interpretations [267]. In this light, the Coolidge effect may be seen as a form of sexual-specific satiety (see chapter SSS).

Origin of Alliesthesia

For the appearance of alliesthesia, at least two sensors and an integrative centre are required: the peripheral sensor detects the environmental stimulus and the internal sensor senses the internal state of the subject. The integrative centre is a ‘comparatory device’ which has ‘prerecorded’ a set-value for the regulated internal parameter concerned. It must be capable of comparing the set value with the real actual value. If alliesthesia is to play a role in physiological regulation, the preceding device must be connected to an ‘adaptatory device’ which in turn can arrange adaptation of the actual value to approach the set value. There are three possible situations: 1, the actual value measured equals the set value: in this case, no response is necessary to guarantee homeostasis of the regulated parameter; 2, and 3, the actual value is above/below the set value: in these cases, the ‘comparatory device’ communicates a signal containing the amount of difference (delta, 〉) and its sign (+/-) to the ‘adaptatory device’.
In temperature regulation (and thermic alliesthesia), hypothalamic sensors [346,347,348,349] measure deep body core temperature, compare it to the set value (normally 36.5°C, elevated in fever, lowered in hypothermia), and, if they do not match, communicate the signed (+/-) difference to motivational brain regions, which in turn interpret the incoming signals, aroused by an external stimulus, as a function of this signed difference and arouse positive or negative sensation. If the external stimulus is appropriate to correct the internal ‘trouble’, CNS hedonic pathways will make this stimulus feel pleasant and appetizing. If the stimulus worsens the situation, it is perceived as unpleasant, if the stimulus is neither beneficial nor noxious, it will be perceived as hedonically neutral. The physiological regulatory response will be autonomic (vasodilatation, sudation/shivering) and behavioral (approach/withdrawal from a source of heat, un/covering…).
The control of food intake follows the same principle, but is more complex, as instead of one regulated parameter (core temperature), there may be many more, although there may be principle ones like plasma glucose (representing metabolizable energy), degradation products of proteins or brain-gut peptides (leptin, NPY…).
Alimentary alliesthesia was demonstrated in subjects prepared with naso-gastric or naso-duodenal tubes in order to exclude olfacto-gustatory stimulation in 1970 [289]. The ‘food’-stimulus, consisting of either a sweet (e.g. sucrose) or salty (NaCl) solution of defined concentration, was infused through the tube directly into the stomach or the upper duodenum. Instead of food-boli arriving successively and over the normal time-span of a meal (15 to 45 min), the solutions were infused at once (as a ‘load’ bolus). The experimental evaluation itself consisted in presenting taste-or odor-samples to the subject prior to the load, which served as a reference-value and then every 5 to 10 min during the ensuing 2 h. Taste samples, consisting of sweet or saline solutions of various concentrations, were not ingested but spat out after giving a hedonic note and the mouth was then rinsed [234,235,285].

Table of contents :

I.􀀃 ABSTRACTS
I.1.􀀃 Summary
I.1.1.􀀃 Keywords
I.2.􀀃 Résumé
I.2.1.􀀃 Mots-clés
II.􀀃 PHYSIOLOGIC CONTROL OF FOOD INTAKE BEHAVIOR
II.1.􀀃 Introduction
II.2.􀀃 ‘Regulation’ or ‘Control’ of food intake?
II.2.1.􀀃 Regulation
II.2.2.􀀃 Control
II.2.3.􀀃 Regulation versus Control
II.3.􀀃 Energy homeostasis
II.4.􀀃 CNS Centers of food intake control
II.4.1.􀀃 The hypothalamus
II.4.2.􀀃 Extra-hypothalamic regions
II.5.􀀃 Peripheral regulation signals
II.5.1.􀀃 Short and long-term signals
II.5.2.􀀃 Digestive signals
II.5.3.􀀃 Hormonal signals
II.6.􀀃 Food intake behavior
II.6.1.􀀃 Periodicity of food intake
II.6.2.􀀃 Episodicity of food intake
II.7.􀀃 Food reward
II.8.􀀃 Unspecific hedonic phenomena
II.8.1.􀀃 Hunger
II.8.2.􀀃 Satiation
II.8.3.􀀃 Satiety
II.8.4.􀀃 The satiety cascade
II.9.􀀃 Specific phenomena
II.9.1.􀀃 Specific hungers & specific appetites
II.9.2.􀀃 PICA
II.9.3.􀀃 Conditioned satiety (CS)
II.9.4.􀀃 Alimentary alliesthesia (AA)
II.9.5.􀀃 Sensory-specific satiety (SSS)
II.10.􀀃 Integration of signals
II.11.􀀃 Environmental and behavioral factors
II.11.1.􀀃 Social, cultural and environmental factors
II.11.2.􀀃 Psycho-affective factors
II.11.3.􀀃 Cognitive factors
II.12.􀀃 Availability and Composition of Food
II.12.1.􀀃 Food availability
II.12.2.􀀃 Food palatability or the ‘appetizer effect’
II.12.3.􀀃 Sensory Variety and Monotony
II.12.4.􀀃 Macronutrient composition
II.12.5.􀀃 Aggregate state of foods
II.12.6.􀀃 Organoleptic properties of food
II.12.7.􀀃 Physical aggressions
III.􀀃 SENSORY PLEASURE: HISTORICAL ASPECTS OF HEDONICS
III.1.􀀃 Ancient Greece
III.2.􀀃 Modern Times
IV.􀀃 MEASUREMENT AND QUANTIFICATION OF REWARD
IV.1.􀀃 Measuring in Humans
IV.1.1.􀀃 Questionnaires
IV.1.2.􀀃 Rating scales
IV.2.􀀃 Measuring in Animals
IV.2.1.􀀃 Visualization and frequency of specific behaviors
IV.3.􀀃 Other Measurement techniques for Animals and Humans
IV.3.1.􀀃 Quantitative Measurement
IV.3.2.􀀃 Choice behavior – Motivational Conflict
IV.3.3.􀀃 Behaviorism and Reward
IV.3.4.􀀃 Facial mimics in newborns
IV.3.5.􀀃 Brain stimulation reward
V.􀀃 ALIMENTARY ALLIESTHESIA
V.1.􀀃 Definition and Terminology
V.2.􀀃 Sensory modalities of alliesthesia
V.2.1.􀀃 Thermal alliesthesia and Alliesthesia for water
V.2.2.􀀃 Olfactory and gustatory alliesthesia
V.2.3.􀀃 Visual and auditory alliesthesia – Environmental alliesthesia
V.2.4.􀀃 Alliesthesia for sexual cues
V.3.􀀃 Origin of Alliesthesia
V.4.􀀃 Mechanism(s) of Alimentary Alliesthesia
V.5.􀀃 Internal signal implicated in Alimentary Alliesthesia
V.5.1.􀀃 Hepatic receptors
V.5.2.􀀃 Intestinal receptors
V.6.􀀃 Specificity of Alimentary Alliesthesia
V.6.1.􀀃 Olfactory alliesthesia
V.6.2.􀀃 Gustatory alliesthesia for primary sense
V.6.3.􀀃 ‘Flavor alliesthesia’?
V.7.􀀃 Time-course and Intensity
V.8.􀀃 Influencing factors
V.8.1.􀀃 Food-related factors
V.8.2.􀀃 Intrinsic and environmental factors
V.8.3.􀀃 Modulation by drugs manipulating reward-circuits
V.9.􀀃 Behavioral equivalent in animals
V.9.1.􀀃 Fish
V.9.2.􀀃 Rats
V.10.􀀃 Innate or acquired?
V.11.􀀃 Functions and finality
V.11.1.􀀃 The ponderostat
V.11.2.􀀃 The function of alimentary alliesthesia
VI.􀀃 SENSORY-SPECIFIC SATIETY (SSS)
VI.1.􀀃 Definition
VI.2.􀀃 Standard test procedure
VI.3.􀀃 Historical aspects
VI.4.􀀃 Sensory modalities
VI.4.1.􀀃 Flavor-specific satiety
VI.4.2.􀀃 Olfactory and taste sensory-specific satiety
VI.4.3.􀀃 Texture-specific satiety
VI.4.4.􀀃 Appearance-specific satiety
VI.4.5.􀀃 Motivation-specific satiety
VI.5.􀀃 Mechanism
VI.5.1.􀀃 Intensity perception: adaptation and habituation
VI.5.2.􀀃 Sensory vs. postabsorptive effects
VI.6.􀀃 CNS mechanisms
VI.6.1.􀀃 CNS studies in non-human primates
VI.6.2.􀀃 CNS studies in humans
VI.6.3.􀀃 Brain systems mediating Liking & Wanting
VI.7.􀀃 Temporal pattern and duration
VI.7.1.􀀃 Short-term SSS
VI.7.2.􀀃 Long-term SSS
VI.8.􀀃 Influencing factors
VI.8.1.􀀃 Weight & Volume
VI.8.2.􀀃 Caloric content
VI.8.3.􀀃 Macronutrients
VI.8.4.􀀃 Variety and Monotony
VI.8.5.􀀃 Aggregate state of foods
VI.8.6.􀀃 Preference
VI.8.7.􀀃 Information on nutrient composition
VI.8.8.􀀃 Dietary restraint and obesity
VI.8.9.􀀃 Alcohol
VI.8.10.􀀃 Age
VI.8.11.􀀃 Eating disorders & pathologies
VI.8.12.􀀃 Innate versus acquired
VI.8.13.􀀃 SSS in rodents
VI.9.􀀃 Purpose and functions
VI.9.1.􀀃 Meal termination
VI.9.2.􀀃 Variety searching
VI.10.􀀃 SSS and the other hedonic phenomena
VI.10.1.􀀃 SSS versus alimentary alliesthesia
VI.10.2.􀀃 SSS versus conditioned satiety
VII.􀀃 EXPERIMENTAL SECTION
VII.1.􀀃 First study: Seasoning
VII.1.1.􀀃 Introduction
VII.1.2.􀀃 Article
VII.1.3.􀀃 Main results & Discussion
VII.2.􀀃 Second study: BMI
VII.2.1.􀀃 Introduction
VII.2.2.􀀃 Article
VII.2.3.􀀃 Main results & Discussion
VII.3.􀀃 Third study: Monotony & Variety
VII.3.1.􀀃 Introduction
VII.3.2.􀀃 Article
VII.3.3.􀀃 Main results & Discussion
VII.4.􀀃 Fourth study: Dishabituation
VII.4.1.􀀃 Introduction
VII.4.2.􀀃 Article
VII.4.3.􀀃 Main results & Discussion
VIII.􀀃 GENERAL CONCLUSIONS ON EXPERIMENTS
VIII.1.􀀃 Conclusions of Study 1
VIII.2.􀀃 Conclusions of Study 2
VIII.3.􀀃 Conclusions of Study 3
VIII.4.􀀃 Conclusions of Study 4
IX.􀀃 GENERAL DISCUSSION
X.􀀃 SUGGESTIONS FOR FUTURE STUDIES
XI.􀀃 REFERENCES
XI.1.􀀃 Chapter Physiological Control
XI.2.􀀃 Chapter Sensory Pleasure
XI.3.􀀃 Chapter Measurement
XI.4.􀀃 Chapter Alliesthesia
XI.5.􀀃 Chapter Sensory-specific satiety
XI.6.􀀃 Chapter Experiments
XII.􀀃 ANNEX – ORIGINAL PUBLICATIONS
XII.1.􀀃 Does modification of olfacto-gustatory stimulation diminish sensory-specific satiety in humans?
XII.2.􀀃 Sensory-specific satiety with simple foods in humans: no influence of BMI?
XII.3.􀀃 Variety enhances food intake in humans: role of sensory-specific satiety.
XII.4.􀀃 Alternation between foods within a meal. Influence on satiation and consumption in humans.

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