November 2004: (II)S193–S204 Smell, Taste, Texture, and Temperature Multimodal Representations in the Brain, and Their Relevance to the Control of Appetite Edmund T. Rolls, DSc The aims of this paper are to describe the rules of cortex is that, in addition to unimodal representations of the cortical processing of taste and smell, how the taste, olfactory, somatosensory, and visual properties the pleasantness or affective value of taste and of sensory stimuli, some neurons combine inputs from smell are represented in the brain, and to relate these different modalities, and these combination-selec- this to the brain mechanisms underlying emotion. tive neurons provide an information-rich representation Much of the fundamental evidence comes from of a wide range of the sensory qualities of food. One key studies in non-human primates, and this is being to understanding these combinatorial representations is complemented by functional neuroimaging stud- ies in humans. learning how individual neurons come to respond to © 2004 International Life Sciences Institute particular combinations of taste, olfactory, texture, and doi: 10.1301/nr.2004.nov.S193–S204 associated visual stimuli. A third processing principle is that the orbitofrontal Introduction cortex represents the pleasantness of taste, olfactory, texture, and associated visual stimuli, as shown by ex- Studies of the brain mechanisms involved in smell and periments in which the activity decreases to zero as food taste are revealing some of the brain processing relevant is fed to satiety, a process that decreases the reward and to understanding how the brain interprets different odors affective value to zero. and tastes. Direct study of the brain activations produced Neuroimaging studies have shown that the human by odor and taste may reveal effects that are not reported orbitofrontal cortex provides a representation of the verbally. It has been shown that approximately 40% of pleasantness of odor. The activation produced by the neurons in the orbitofrontal cortex taste and olfactory odor of a food eaten to satiety decreases relative to areas provide a representation of odor that depends on another food-related odor not eaten in the meal. In the the taste with which the odor has been associated previ- ously, and that this representation is produced by a same general area, there is a representation of the pleas- slowly acting learning mechanism. Other neurons in the antness of the smell, taste, and texture of a whole food. orbitofrontal cortex respond to the odor and to sensory Activation in this area decreases to a food eaten to information about the texture of food in the mouth satiety, but not to a food that has not been eaten in the (including the mouth feel of fat) and some respond to the meal. With neuroimaging it is possible to show that viscosity of what is in the mouth. The representation of pleasant and unpleasant odors activate different regions odor thus moves beyond the domain of physicochemical of the orbitofrontal cortex and cingulate cortex. It has properties of odors to a domain where the ingestion- also been shown that the combination of monosodium related significance of the odor determines the represen- glutamate (MSG) and inosine monophosphate (IMP), tation provided by some neurons. which together produce an enhanced umami taste qual- Another processing principle in the orbitofrontal ity, result in supralinear activation of a part of the anterior orbitofrontal cortex, reflecting an effect of the combination of these two stimuli. Dr. Rolls is with the University of Oxford, Depart- Studies of the brain activation produced by odors ment of Experimental Psychology, Oxford, England. and tastes are thus revealing some of the principles of the Address for correspondence: University of Ox- representation of odor and taste in the brain, and also ford, Department of Experimental Psychology, South Parks Road, Oxford OX1 3UD, United Kingdom; indicate that brain correlates of the acceptability and Phone: 44-1865-271348; Fax: 44-1865-310447; E-mail: pleasantness of odors and tastes can be provided by [email protected]. neuroimaging. A broad perspective on brain processing Nutrition Reviewsா, Vol. 62, No. 11 S193 involved in emotion is provided in a book entitled The modal regions is documented below. The multimodal Brain and Emotion.1 convergence that enables single neurons to respond to different combinations of taste, olfactory, texture, tem- Taste Processing in the Primate Brain perature, and visual inputs to represent different flavors Pathways. A diagram of the taste and related olfac- produced often by new combinations of sensory input is tory, somatosensory, and visual pathways in primates is a theme of recent research. shown in Figure 1. In primates there is a direct projection The Secondary Taste Cortex. A secondary cortical from the rostral part of the nucleus of the solitary tract to taste area in primates was discovered in the caudolateral the taste thalamus and thus to the primary taste cortex in orbitofrontal cortex, extending several millimeters in the frontal operculum and adjoining insula, with no front of the primary taste cortex.4 One principle of taste pontine taste area and associated subcortical projections processing is that by the secondary taste cortex, the as in rodents.2,3 This emphasis on cortical processing of tuning of neurons can become quite specific, with some taste may be related to the great development of the neurons responding, for example, only to sweet taste. cerebral cortex in primates, and the advantage of using This specific tuning (especially when combined with extensive and similar cortical analysis of inputs from olfactory inputs) helps to provide a basis for changes in every sensory modality before the analyzed representa- the appetite for some but not other foods eaten during a tions from each modality are brought together in multi- meal. Figure 1. Schematic diagram of the taste and olfactory pathways in primates showing how they converge with each other and with visual pathways. The gate functions shown refer to the finding that the responses of taste neurons in the orbitofrontal cortex and the lateral hypothalamus are modulated by hunger. VPMpc ϭ Ventralposteromedial thalamic nucleus; V1, V2, V4 ϭ visual cortical areas. S194 Nutrition Reviewsா, Vol. 62, No. 11 Five Prototypical Tastes, Including Umami. In the primary and secondary taste cortex, there are many neurons that respond best to each of the four classical prototypical tastes—sweet, salt, bitter, and sour5—but there are also many neurons that respond best to umami tastants such as glutamate (which is present in many natural foods such as tomatoes, mushrooms, and milk6) and IMP (which is present in meat and some fish such as tuna7). This evidence, together with the identification of a glutamate taste receptor,8 leads to the view that there are five prototypical types of taste information channels, with umami contributing—often in combination with corresponding olfactory inputs9—to the flavor of protein. The Pleasantness of the Taste of Food. The modu- lation 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 behavior is controlled.1 The subjective correlate of this Figure 2. The effect of feeding to satiety with glucose solution modulation is that food tastes pleasant when we are on the responses of two neurons in the secondary taste cortex to hungry and tastes hedonically neutral when it has been the taste of glucose and of black currant juice (BJ). The spontaneous firing rate is also indicated (SA). Below the eaten to satiety. We have found that the modulation of neuronal response data for each experiment, the behavioral taste-evoked signals by motivation is not a property measure of the acceptance or rejection of the solution on a scale found in the early stages of the primate gustatory system. from ϩ2 to –2 (see text) is shown. The solution used to feed to The responsiveness of taste neurons in the nucleus of the satiety was 20% glucose. The monkey was fed 50 mL of the solitary tract10 and in the primary taste cortex, the frontal solution at each stage of the experiment, as indicated along the opercular,11 and the insular cortex,12 is not attenuated by abscissa, until he was satiated, as shown by whether he ac- cepted or rejected the solution. Pre ϭ Firing rate of the neuron feeding to satiety. In contrast, in the secondary taste before the satiety experiment started. The values shown are the cortex, in the caudolateral part of the orbitofrontal cor- mean firing rate and its standard error. (From Rolls et al.13) tex, it has been shown that the responses of the neurons to the taste of glucose decreased to zero while the monkey ate it to satiety, during the course of which the 14-20 behavior turned from avid acceptance to active rejec- reduction in the pleasantness of its taste, are not tion.13 This modulation of responsiveness of the gusta- produced by a reduction in the responses of neurons in tory responses of the orbitofrontal cortex neurons by the nucleus of the solitary tract or frontal opercular or satiety could not have been due to peripheral adaptation insular gustatory cortices to gustatory stimuli. Indeed, in the gustatory system or to altered efficacy of gustatory after feeding to satiety, humans reported that the taste of stimulation after satiety was reached, because modula- the food with which they had been satiated tasted almost tion of neuronal responsiveness by satiety was not seen as intense as when they were hungry, though much less 21 at the earlier stages of the gustatory system, including the pleasant. This comparison is consistent with the possi- nucleus of the solitary tract, the frontal opercular taste bility that activity in the frontal opercular and insular cortex, and the insular taste cortex.