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Food ingestion induces a metered response of the digestive system. Initially, the upper digestive system reacts to process and extract meal substrates. Later, meal residues not absorbed in the small bowel, pass into the colon and activate the metabolism of resident microbiota. Food consumption also induces sensations that arise before ingestion (e.g., anticipatory reward), during ingestion (e.g., gustation), and most importantly, after the meal (i.e., the postprandial experience). The postprandial experience involves homeostatic sensations (satiety, fullness) with a hedonic dimension (digestive well-being, mood). The factors that determine the postprandial experience are poorly understood, despite their potential role in personalized diets and healthy eating habits. Current data suggest that the characteristics of the meal (amount, palatability, composition), the activity of the digestive system (suited processing), and the receptivity of the eater (influenced by multiple conditioning factors) may be important in this context.
Keywords: food ingestion, digestion, satiety, digestive well-beingThe importance of a healthy diet is well recognized, but to become acceptable, a diet needs to be attractive and gratifying. In this regard, it is crucial to understand the factors that determine the responses to ingested food and in particular the lasting effects following ingestion, i.e., the postprandial experience. In this context, the Nutrients Special Issue entitled Food and Diet for Gut Function and Dysfunction focuses on the role of the responses of the digestive system to food ingestion in normal conditions and in the disease state. The aim of the present paper is to provide an introductory overview to the Special Issue, outlining the effects of food ingestion on the brain-gut axis, i.e., the relations between digestive responses and the sensory experience. Purposely, this review is sketchy and descriptive; most of the experimental factual/information is provided in the different articles that compose the Special Issue. A comprehensive review on this subject, analyzing the relations between gastronomy and neurogastroenterology, has been previously published [1].
During fasting, the gastrointestinal tract exerts a cyclic activity, alternating between periods of quiescence and periods of intense motor and secretory activity. The function of this stereotyped pattern, known as the migrating motor complex (MMC), appears to be the propulsion of residues from the lumen of the small intestine into the colon; thus, it is considered to be the intestinal housekeeper [2].
With the initiation of a meal, the digestive system is stimulated leading to the suppression of the interdigestive motor pattern and the activation of the digestive process. The digestive process involves three semi-sequential phases that overlap over time: cephalic, luminal, and post-absorptive. The cephalic phase refers to events before and during the ingestion period. Indeed, even before ingestion, the digestive system starts with a series of preparatory procedures, associated in normal conditions with an anticipatory reward sensation, e.g., anticipation of a desired meal stimulates salivary and gastric secretion. Food ingestion and swallowing activate oropharyngeal and oesophagogastric responses (salivation, oesophageal peristalsis, and gastric receptive relaxation). The walls of the stomach are contracted and virtually collapsed during fasting and meal arrival into the stomach induces an active relaxation (gastric accommodation). Solid particles activate the antral pump with peristaltic activity, which starts a grinding process that transforms the meal into a liquid chime. A gradual re-contraction of the stomach during the postprandial phase pushes the chime into the small bowel [3]. The activity of the stomach and small bowel adapts to the requirements of the digestive process, so that, food is digested and subsequently absorbed by a sequence of complex physical and chemical processes that begin in the mouth and extend to the terminal ileum. Ultimately, non-absorbed residues reach the colon [4]; these dietary residues serve as substrates for gut microbiota, and in return, the gut microbiota can affect host physiology and digestive function ( Figure 1 ).
Digestive response to ingestion. The upper digestive system extracts meal substrates by a process of digestion and absorption. Non-absorbed meal residues pass into the colon and feed the microbiota.
Indeed, the large majority of human microbiota inhabit the colon, which provides a dedicated niche for this population of symbiotic organisms. Microbiota fermentation of meal residues releases a series of metabolites that, in turn, serve as substrates for other subsets of microbiota. Hence, the colon contains a biomass formed by microbiota, meal residues, and secondary metabolic products in a dynamic chain of metabolic reactions. The total volume of colonic biomass consists of approximately 500–800 mL with a 30% daily turnover (100–200 mL daily fecal output) [5]. Microbiota metabolism of some meal residues releases gas; hence, colonic gas production reflects microbiota metabolic activity [6]. Approximately 100 min after ingestion, unabsorbed residues start arriving into the colon, and gas production increases. The plateau lasts approximately 4–6 h depending on the meal composition and then gradually declines [7], but the effect persists as long as substrates remain available, such that the residue loads of consecutive meals contribute to gas production [8]. The volume of gas produced within 6 h after a meal ranges from 200 mL with a standard breakfast to 600 mL with a flatulogenic meal [7].
The activity of the muscles of the abdominal and thoracic walls depends on its content. Specifically, an increase in intraabdominal volume induces an adaptive relaxation of the diaphragm, which allows orad expansion of the abdominal cavity with compensatory contraction of the anterior abdominal wall; this somatic response prevents an increment in abdominal girth. The same adaptive response is triggered by ingestion of a meal, a phenomenon termed abdominal accommodation [9]. The extent of accommodation depends on the volume load. This somatic reflex has clinical relevance, because impaired abdominal accommodation produces abdominal distension, a frequent complaint in clinical practice; in these patients, an abnormal contraction of the diaphragm pushes abdominal content with protrusion of the anterior abdominal wall [10]. Physiologic changes in blood pressure, heart rate, blood flow in the superior mesenteric artery, and mesenteric vascular resistance, as well as in thermogenesis are also induced during the luminal and post-absorptive phase of digestion, but the specific meal-derived signals that control these responses are incompletely understood [11].
The entire digestive-absorptive process is finely regulated by a complex net of neuro-humoral feedback mechanisms, by which the gut is able to sense and react to intraluminal stimuli [4]. These reflex pathways are distributed within the autonomic and the enteric nervous system. This physiological configuration allows the gut to be highly versatile and adaptable. Stimuli in the gut may also activate afferent brain pathways, so that in addition to the digestive responses, meal consumption also induces sensory experiences that influence the control of food consumption and homeostasis (e.g., fullness and satiety) [12,13,14,15,16,17]. These sensory experiences are associated with pleasant or occasionally unpleasant sensations (changes in mood and digestive well-being), i.e., the hedonic dimension of the sensory experience [12,13,14,18,19]. Changes in the activity of the central nervous system (CNS) in response to meal ingestion have been documented by means of functional brain imaging (e.g., functional magnetic resonance imaging and positron emission tomography) [20,21,22,23,24,25,26]. These studies reveal the crucial role of the CNS in the control of food intake and the conscious perception of sensation and in the maintenance of homeostasis [27]. Meal ingestion is associated with changes in the blood levels of several compounds [13,28,29,30]. These compounds may be derived directly from the food (e.g., amino acids, lipids, and glucose), produced by the organism in response to the meal (e.g., hormones and neuropeptides) or may be the result of the metabolism of non-absorbed residues by the colonic microbiota [31,32]. The bidirectional interaction between the mind and the digestive system, involving both neural and humoral pathways is known as the brain–gut (or gut–brain) axis. There is a dynamic cross-talk between host and microbiota, the messengers and circuits are poorly understood, but metabolites derived from microbiota activity may play a role [33]. Attending to the role of microbiota, the concept has been extended to encompass the microbiota–gut–brain axis.
The biological response to food is complex and involves events before, during, and after the meal. Indeed, the sensory experience related to meals starts before the ingestion period [34]. The anticipatory experience before the meal depends on factors related to the meal (e.g., meal appearance, smell), as well as the subject’s homeostatic status (e.g., degree of hunger) and cognitive state (e.g., expectations).
Appetite is an imprecise term, since it may refer to differing concepts. It can be used as an all-inclusive term to cover all aspects of food intake, preference, motivation, and selection, or as a reference to the sensory and qualitative aspects of eating and the responsiveness to environmental stimulation [16]. Thus, the concept of “meal wanting” was coined in order to describe the pre-ingestive response to a specific food, i.e., the desire to eat that particular product [35,36].
The motivational aspect of food consumption has been the subject of numerous studies [18,37,38,39,40]. The homeostatic regulation of eating depends on the degree of hunger (or satiation). Food ingestion reduces hunger sensation and depending on the amount ingested, induces satiation and fullness sensations; in principle satiation is a signal to stop ingestion. Remarkably, satiation is taste-specific, thus food diversity increases meal consumption. In any case, with increasing satiety and fullness, “meal wanting” and the desire to eat a food of choice decrease. The homeostatic regulation of food ingestion might be overruled by other factors such as the hedonic drive; this may lead to excessive eating and it has been associated with obesity and eating disorders [41,42]. Cognitive factors and the habits of the subject also play an important role. These include memories, beliefs, expectations, and thoughts related to what the subject considers about (a) the characteristics of the meal (satiating capacity, quality, health properties); (b) meal availability, either present and/or in the near future; (c) what the eater believes is beneficial or necessary at a certain moment (e.g., low-fat food for an obese patient). Notwithstanding, a decisive factor on food consumption is, at the end, what is present in the menu or in the plate, and thus, the importance of the serving portions in food consumption.
The most important aspects of food that can be detected by the senses (organoleptic properties) are taste, smell, and texture, although other properties, such as temperature, sound, and appearance, are also involved. The biology and physiologic mechanisms of food sensation have been thoroughly studied [43,44,45,46]. For the purpose of this review, three concepts in this regard will be considered: taste, flavor, and palatability
The taste perception, or in other words gustation, is triggered by the stimulation of specific receptors in the mouth and in the pharynx by molecules in a liquid environment. The five tastes that are widely accepted to play a major role in the experience of sensing food are: salty, sour, umami, bitter, and sweet. However, many additional tastes (~20) including fatty acid, metallic, and electric have been proposed as candidates [47,48]. Nevertheless, the specific receptors involved in sensing each taste are still not fully understood. Moreover, the distribution and number of taste buds may differ in different persons as shown by the extreme sensitivity to bitter taste secondary to increased number of taste buds in up to 25% of the population, these individuals can be considered as supertasters [49,50]. Interestingly, taste receptors similar to those responsible for food sensing in the mouth have been identified along the gastrointestinal tract; their function appears to be related to regulation of gut function and homeostasis independent form taste sensation [3,51,52,53,54].
Flavor is a complex and multi-modal sensory experience that occurs during food tasting [43] and directly involves gustatory and olfactory sensations [55]. However other senses, such as proprioception, temperature, vision, and sound, can impact flavor perception. Consequently, flavor is a combined interoceptive and exteroceptive experience.
The hot sensation in spices (pungency) is produced by capsaicin and other chemical components. These molecules are not sensed by taste receptors, but by sensory nerve endings analogous to those signaling pain, and the sensation is driven by the trigeminal nerves. Pungency is an important aspect in the flavor of food.
Olfaction, i.e., the perception of smell, deeply interacts with and enhances the perception of taste. The process of olfaction involves the orthonasal and retronasal systems. The former is activated by inhaling volatile compounds that enter the nose via the nostrils, while the latter is activated by volatile compounds released from the food during chewing and swallowing that reach the retronasal system through the posterior nares when the individual exhales. Sensory inputs form the anterior and posterior nasal systems are transmitted through different neural pathways to different brain areas. There are roughly 500 types of odorant receptors in the nasal mucosa [56,57,58]. Certain molecules activate several types of receptors, while each receptor type may be activated by different molecules. Thus, the precise odor of a product depends on the mixture of activated receptors.
Food temperature influences taste since it regulates the access of molecules from volatile compounds to sensing receptors. Moreover, in some individuals, sweet, sour, bitter, or salty sensations can be evoked by the application of heat to different parts of the tongue; a characteristic known as “thermal taster”.
Food texture is perceived by touch and proprioception and depends on the rheological properties of the meal (i.e., flow of matter/changes in matter in response to applied force). Important hints to the texture of the meal are obtained before ingestion by physical manipulation (cutting, touching, mixing), vision, and occasionally by sound. During the oral phase, the feel of the food (mouth feel) is sensed by mastication and tongue shearing. Also, the sound that food makes within the mouth (e.g., crispy fries or crunchy crackers) is important for flavor sensing. There is an almost endless combination of textures that can be present in a meal (e.g., elasticity, consistency, astringency, viscosity, granularity, smoothness, sogginess, etc.).
Food appearance is an important factor that shapes the expectations related to flavor. Indeed, in a very interesting study, experimental mismatch of color in fruit-flavored beverages and candies was associated with incorrect identification of the product, (e.g., a yellow candy tends to be recognized as lemon flavor regardless of the true taste) [59]. It should be noted that mastication, salivation, and tongue movement change the rheological properties of food and molecules activating taste and smell are widely spread in the oral and retronasal cavities. Hence, the oral phase of digestion modifies the interoceptive properties of food that determine flavor (taste, odor, texture, pungency, and temperature).
Palatability it is not a characteristic of the food itself, but rather it refers to the hedonic sensation (pleasurable or aversive) derived from food tasting (i.e., how good the food is perceived) [60]. It depends on the organoleptic properties of the meal, but more importantly on the receptiveness of the eater: the state of the eater before the meal (e.g., hunger), flavor perception, and interpretation [61,62]. Consequently, the palatability of the meal is dynamic and it changes during ingestion (palatability decreases as hunger decays and satiation arises). Subject attentiveness also plays an important role, e.g., palatability is more pronounced when the subject is paying attention to the meal than when distracted. The notion of “meal liking”, in contrast to “meal wanting”, reflects the hedonic dimension of the gustatory experience, i.e., palatability, but it extends further to include the postprandial sensation of satisfaction and digestive well-being [35]. Previous experience and memory influence palatability, such that more palatability is associated to flavors that are congruent and recognized. Conversely, exposure to an unfamiliar or aversive flavor can translate into a decrease in palatability [46]; however, in special situations (e.g., dinner in a special restaurant) the receptivity of the subject is increased and an unrecognized, unexpected, or incongruent gustatory experience (e.g., cold soup, salty ice cream) may increase the palatability of the meal by the surprise factor.
The sensations that arise during the time of ingestion extend into the postprandial period. Hence, the postprandial experience comprises homeostatic sensations (satiation, fullness) and hedonic sensations (i.e., post-prandial mood and digestive well-being) ( Figure 2 ).
