Sensory processing in the brain related to the control of food intake

Abstract

Complementary neurophysiological recordings in rhesus macaques (Macaca mulatta) and functional neuroimaging in human subjects show that the primary taste cortex in the rostral insula and adjoining frontal operculum provides separate and combined representations of the taste, temperature and texture (including viscosity and fat texture) of food in the mouth independently of hunger and thus of reward value and pleasantness. One synapse on, in the orbitofrontal cortex, these sensory inputs are for some neurons combined by learning with olfactory and visual inputs. Different neurons respond to different combinations, providing a rich representation of the sensory properties of food. In the orbitofrontal cortex feeding to satiety with one food decreases the responses of these neurons to that food, but not to other foods, showing that sensory-specific satiety is computed in the primate (including the human) orbitofrontal cortex. Consistently, activation of parts of the human orbitofrontal cortex correlates with subjective ratings of the pleasantness of the taste and smell of food. Cognitive factors, such as a word label presented with an odour, influence the pleasantness of the odour, and the activation produced by the odour in the orbitofrontal cortex. Food intake is thus controlled by building a multimodal representation of the sensory properties of food in the orbitofrontal cortex and gating this representation by satiety signals to produce a representation of the pleasantness or reward value of food that drives food intake. Factors that lead this system to become unbalanced and contribute to overeating and obesity are described.Sensory-specific satiety: Fat: Food texture: Taste: OlfactionThe aims of the present paper are to describe the rules of the cortical processing of taste and smell, how the pleasantness or affective value of taste and smell are represented in the brain, and to relate this information to the brain mechanisms underlying the control of appetite, food intake and obesity. To make the results relevant to understanding the control of human food intake, complementary evidence is provided by neurophysiological studies in non-human primates and by functional neuroimaging studies in human subjects. A broad perspective on brain processing involved in emotion and in hedonic aspects of the control of food intake is provided by Rolls (2005a). Taste processing in the primate brain PathwaysA diagram of the taste and related olfactory, somatosensory and visual pathways in primates is shown in Fig. 1. The multimodal convergence that enables single neurons to respond to different combinations of taste, olfactory, Abbreviation: fMRI, functional magnetic resonance imaging.

Taste, olfactory and food texture reward processing in the brain and obesity

“…The satiety signals that help in this modulation may reach the OFC from the hypothalamus, and in turn, the OFC projects to the hypothalamus in which neurons are found that respond to the sight, smell and taste of food if hunger is present. 22,23 We have observed above some of the principles that help to make the food pleasant, including particular combinations of taste, olfactory, texture, visual, and cognitive inputs. I develop a hypothesis below (in the section 'Brain processing of the sensory properties and pleasantness of Pleasantness ratings % BOLD change Figure 4 Effect of paying attention to the pleasantness vs the intensity of a taste stimulus.…”

“…[85][86][87][88] There are many factors that can cause or contribute to obesity in humans [89][90][91] that are analyzed with approaches within or related to neuroscience and psychology. 1,23,92,93 Rapid progress is being made in understanding many of these factors at present with the aim of leading to better ways to minimize and treat obesity. These factors include the following:…”

“…17,[20][21][22] The pleasantness of the taste of food sensory-specific satiety and the effects of variety on food intake The modulation of the reward value of a sensory stimulus such as the taste of food by motivational state, for example, hunger is one important way in which motivational behaviour is controlled. 1,23 The subjective correlate of this modulation is that food tastes pleasant when hungry and tastes hedonically neutral when it has been eaten to satiety. Following Edmund Rolls' discovery of sensory-specific satiety revealed by the selective reduction in the responses of lateral hypothalamic neurons to a food eaten to satiety, 24,25 it has been shown that this is implemented in a region that projects to the hypothalamus, the orbitofrontal (secondary taste) cortex, for the taste, odour and sight of food.…”

Self-regulatory depletion in dogs: Insulin release is not necessary for the replenishment of persistence

“…Thus, it has been suggested that the oral detection of glucose by taste receptors replenishes by stimulating areas of the brain that and the ventral striatum (Chambers et al, 2009), which are two regions of the brain involved in the representation of food rewards (Rolls, 2007), and are likewise involved in the motivation and regulation of goal-oriented behavior (Holroyd and Yeung, 2012;Harsay et al, 2011). Glucose also elicits the release of dopamine in the medial prefrontal cortex (Touzani et al, 2010).…”

Genetic influences on dietary variety - Results from a twin study

“…Thus, people who satiate more quickly to a particular taste may be more prone to seek greater diversification in their diet across a given period of time (Addessi, Mancini, Crescimbene, Ariely, & Visalberghi, 2010;Epstein, Temple, Roemmich, & Bouton, 2009;Pessemier, 1985;Van Trijp, 1994). However, even though sensory-specific satiety has a strong biological basis and is relatively stable over time (Rolls, 2007), it usually refers to similarities of specific food attributes, including taste, appearance, smell, and texture, that are presented within a short time frame (Hetherington, Rolls, & Burley, 1989;Rolls et al, 1981). Thus, it is not clear how far it relates to variety seeking on the level of food items that are consumed over an extended period of time, which is the focus of this paper.…”