The interplay between mouth and mind : explaining variation in taste-related brain activation

Food does not always ‘taste’ the same. During hunger, for example, food may be tastier compared to during satiety. Many other internal and external factors affect the way we experience our food and make it a dynamic process. Our brain is responsible for weighing and integrating these factors and forms the final consumption experience. Mapping the impact of all factors that influence the consumption experience is of fundamental importance for understanding why we eat the way we eat. Important drivers for food consumption are its rewarding capacity, healthiness and caloric content. Furthermore, in the current supermarket environment, advertisements and food claims are omnipresent, and may exert influence on our consumption experience by triggering all kinds of cognitive processes. Therefore, in this thesis we aimed to assess the effect of food content (caloric content and sugar type), character (personality trait reward sensitivity and attitude health-interest) and cognitive effects (labeling/claim effects and selective attention to food properties) on brain activation during tasting. Such taste-related brain responses were obtained with the use of functional Magnetic Resonance Imaging while administering small sips of liquid to young, normal weight female participants in a MRI scanner.

To begin with, we focussed on the effect of caloric content on taste responses (Chapter 2). An important function of eating is ingesting energy, and the ability to sense energy in the oral cavity would therefore be biologically relevant. However, in this thesis we showed that oral exposure to caloric (maltodextrin and maltodextrin + sucralose) and non-caloric (sucralose) stimuli does not elicit discriminable responses in the brain when averaged over hunger and satiety. Nevertheless, energy content did interact with hunger state in several brain regions involved in inhibition (approach-avoidance behaviors) and gustation: the middle cingulate cortex, ventrolateral prefrontal cortex, anterior insula and thalamus. Thus, brain activation in response to oral calories, irrespective of sweetness, seems to be dependent on hunger state.

In addition to the detection of oral calories in general, we examined whether different sugar types, glucose and fructose, can be sensed in the oral cavity (Chapter 3). Tasting glucose compared to fructose evoked greater food reward (anterior cingulate cortex, ACC) activation during hunger and greater food motivation (precentral gyrus) activation during hunger and satiety. Responses to oral fructose relative to glucose were greater only during satiety in an area associated with inhibitory control (superior frontal gyrus). It appears that oral glucose and fructose evoke differential brain responses, independent of sweetness.

Secondly, we investigated in how far reward sensitivity, a personality trait, affected brain responses to calories in the oral cavity (Chapter 4). This because a food’s reward value is highly dependent on its caloric content. Sensitivity to rewards was measured with the Behavioral Activation System Drive scale and was correlated with oral calorie activation from a simple maltodextrin solution and a sucrose sweetened soft drink. Oral calorie activation was obtained by subtracting activation by a non-caloric solution (sucralose solution/non-caloric soft drink) from that by a caloric solution (maltodextrin + sucralose/sucrose sweetened soft drink). We found that neural responses to oral calories from a maltodextrin solution are modulated by reward sensitivity in reward-related areas such as the caudate, amygdala, and ACC. For soft drinks, we found no correlations with reward sensitivity in any reward related area. This discrepancy may be due to the direct detection of maltodextrin, but not sucrose in the oral cavity. However, the absence of this effect in a familiar soft drink warrants further research into its relevance for real life ingestive behavior.

In the last part of this thesis we explored how cognitions modulate the consumption experience. Perceived, rather than actual caloric content, inflicted by calorie food labels, induces cognitive processes that may influence the consumption experience on their own. We tested this in an experiment and found that receipt of a beverage perceived as low- compared to high-caloric induced more activation in the dorsal striatum, a region involved in coding food reward (Chapter 5). As low-calorie labels may appeal especially to the health-minded consumers, we correlated brain responses to the receipt of a beverage perceived as low- compared to high-caloric with health interest (measured with the General health interest subscale of the Health and Taste Attitude Scales). Indeed, health interest scores correlated positively with activation in the dorsal striatum.

Rather than focussing participants’ attention on differences within one food aspect, in Chapter 6 we focussed on selective attention to different food aspects, i.e. pleasantness versus taste intensity versus calories. In the supermarket, food labels and claims often do the same. In the first place, paying attention to hedonics, caloric content or taste intensity predominantly resulted in common brain activation in regions involved in the neural processing of food stimuli, e.g. the insula and thalamus. This likely resulted from ‘bottom-up’ sensory effects, which are more prominent than ‘top-down’ attentional effects. However, small differences were also observed; taste activation was higher during selective attention to intensity compared to calories in the right middle orbitofrontal cortex and during selective attention to pleasantness compared to intensity in the right putamen, right ACC and bilateral middle insula. Overall, these results indicate that statements regarding food properties can alter the consumption experience through attention-driven effects on the activation of gustatory and reward regions.

Finally, the general discussion (Chapter 7) describes main finding and conclusions of this thesis. In sum, we showed that food energy content, sugar type, trait reward sensitivity, health interest, food labels and selective attention all modulate taste-related brain activation. In conclusion, these findings indicate that the formation of the final consumption experience is a very multifaceted process that dependents on numerous factors integrated by the brain, of which we are just beginning to grasp its complexity.