How Pleasant and Unpleasant Stimuli Combine in Different Brain Regions: Odor Mixtures

Abstract

Many affective stimuli are hedonically complex mixtures containing both pleasant and unpleasant components. To investigate whether the brain represents the overall affective value of such complex stimuli, or the affective value of the different components simultaneously, we used functional magnetic resonance imaging to measure brain activations to a pleasant odor (jasmine), an unpleasant odor (indole), and a mixture of the two that was pleasant. In brain regions that represented the pleasantness of the odors such as the medial orbitofrontal cortex (as shown by activations that correlated with the pleasantness ratings), the mixture produced activations of similar magnitude to the pleasant jasmine, but very different from the unpleasant indole. These regions thus emphasize the pleasant aspects of the mixture. In contrast, in regions representing the unpleasantness of odors such as the dorsal anterior cingulate and midorbitofrontal cortex the mixture produced activations that were relatively further from the pleasant component jasmine and closer to the indole. These regions thus emphasize the unpleasant aspects of the mixture. Thus mixtures that are found pleasant can have components that are separately pleasant and unpleasant, and the brain can separately and simultaneously represent the positive and negative hedonic value of a complex affective stimulus that contains both pleasant and unpleasant olfactory components. This type of representation may be important for affective decision making in the brain in that separate representations of different affective components of the same sensory stimulus may provide the inputs for making a decision about whether to choose the stimulus or not.

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

“…22,62 The primary olfactory (pyriform) cortex represents the identity and intensity of odour in that activations there correlate with the subjective intensity of the odour, and the orbitofrontal and ACC represents the reward value of odour, in that activations there correlate with the subjective pleasantness of odour. 22,62,63 Olfactory-taste convergence to represent flavour and the influence of satiety Supradditive effects indicating convergence and interactions were found for taste (sucrose) and odour (strawberry) in the orbitofrontal and ACC, and activations in these regions were correlated with the pleasantness ratings given by the participants. [64][65][66] These results provide evidence on the neural substrate for the convergence of taste and olfactory stimuli to produce flavour in humans, and where the pleasantness of flavour is represented in the human brain.…”

A common neural scale for the subjective pleasantness of different primary rewards

“…Each experimental stimulus was presented in permuted sequence 12 times. This general protocol and design have been used successfully in previous studies to investigate activations and their relation to subjective ratings in cortical areas (de Araujo et al, 2005;Grabenhorst et al, 2007;Rolls et al, 2003a).…”

“…The pleasantness and intensity ratings were used as subject-specific regressors for neural activations to find brain regions that track the subjective pleasantness or the subjective intensity of the temperature and taste rewards. This method of using subjective ratings as regressors for neural activations has previously been used to successfully identify brain areas where activity reflects the subjective affective value of stimuli when value is altered by presenting a range of affective stimuli or by feeding subjects to satiety Grabenhorst et al, 2007;Kringelbach et al, 2003).…”

“…Support for some role of the anterolateral orbitofrontal cortex in reward processing is that in an investigation with hedonically complex odor stimuli that included positive and negative components, activations were correlated with subjective pleasantness in the anterolateral orbitofrontal cortex [40 52 -6] (Grabenhorst et al, 2007). Further, encoding of the relative pleasantness of olfactory stimuli was found in the A C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPT 20 anterolateral orbitofrontal cortex [-38 48 -12] by ); activations to pleasant odors (but not to unpleasant odors) have been reported in the anterolateral orbitofrontal cortex [-42 42 -12] (Royet et al, 2003); and in a monetary reward/loss task, activations in the anterolateral orbitofrontal cortex were related to reward minus loss [-39 42 -15] (O'Doherty et al, 2003a).…”

“…Brain imaging can then be used to identify regional activations that correlate with these ratings. Using this approach, neural representations of the subjective pleasantness of different types of rewards have been found in brain areas including the orbitofrontal Grabenhorst et al, 2007;Kringelbach et al, 2003) and anterior cingulate cortices Grabenhorst et al, 2007;McCabe and Rolls, 2007). However, none of these investigations has directly tested whether the same brain area represents the subjective pleasantness of qualitatively different rewards on a common neural scale.…”