Functions of the orbitofrontal and pregenual cingulate cortex in taste, olfaction, appetite and emotion.
Complementary neurophysiological recordings in macaques and functional neuroimaging in humans 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. The representation of taste and other food-related stimuli in the orbitofrontal cortex of macaques is found from its lateral border throughout area 13 to within 7 mm of the midline, and in humans the representation of food-related and other pleasant stimuli is found particularly in the medial orbitofrontal cortex. 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 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 which drives food intake. A neuronal representation of taste is also found in the pregenual cingulate cortex, which receives inputs from the orbitofrontal cortex, and in humans many pleasant stimuli activate the pregenual cingulate cortex, pointing towards this as an important area in motivation and emotion.
Rolls
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Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD, England. Edmund.Rolls@psy.ox.ac.uk
D000818:Animals; D001066:Appetite / Q000502:physiology*; D001931:Brain Mapping; D004644:Emotions / Q000502:physiology*; D005625:Frontal Lobe / Q000166:cytology / Q000502:physiology*; D006179:Gyrus Cinguli / Q000166:cytology / Q000502:physiology*; D006801:Humans; D009434:Neural Pathways / Q000166:cytology / Q000502:physiology; D009474:Neurons / Q000502:physiology; D012528:Satiety Response / Q000502:physiology; D012903:Smell / Q000502:physiology*; D013649:Taste / Q000502:physiology*