Ivan E. de Araujo

Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain.

The functional architecture of the central taste and olfactory systems in primates provides evidence that the convergence of taste and smell information onto single neurons is realized in the caudal orbitofrontal cortex (and immediately adjacent agranular insula). These higher‐order association cortical areas thus support flavour processing. Much less is known, however, about homologous regions in the human cortex, or how taste–odour interactions, and thus flavour perception, are implemented in the human brain. We performed an event‐related fMRI study to investigate where in the human brain these interactions between taste and odour stimuli (administered retronasally) may be realized. The brain regions that were activated by both taste and smell included parts of the caudal orbitofrontal cortex, amygdala, insular cortex and adjoining areas, and anterior cingulate cortex. It was shown that a small part of the anterior (putatively agranular) insula responds to unimodal taste and to unimodal olfactory stimuli, and that a part of the anterior frontal operculum is a unimodal taste area (putatively primary taste cortex) not activated by olfactory stimuli. Activations to combined olfactory and taste stimuli where there was little or no activation to either alone (providing positive evidence for interactions between the olfactory and taste inputs) were found in a lateral anterior part of the orbitofrontal cortex. Correlations with consonance ratings for the smell and taste combinations, and for their pleasantness, were found in a medial anterior part of the orbitofrontal cortex. 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.

Different representations of pleasant and unpleasant odours in the human brain

Odours are important in emotional processing; yet relatively little is known about the representations of the affective qualities of odours in the human brain. We found that three pleasant and three unpleasant odours activated dissociable parts of the human brain. Pleasant but not unpleasant odours were found to activate a medial region of the rostral orbitofrontal cortex. Further, there was a correlation between the subjective pleasantness ratings of the six odours given during the investigation with activation of a medial region of the rostral orbitofrontal cortex. In contrast, a correlation between the subjective unpleasantness ratings of the six odours was found in regions of the left and more lateral orbitofrontal cortex. Moreover, a double dissociation was found with the intensity ratings of the odours, which were not correlated with the BOLD signal in the orbitofrontal cortex, but were correlated with the signal in medial olfactory cortical areas including the pyriform and anterior entorhinal cortex. Activation was also found in the anterior cingulate cortex, with a middle part of the anterior cingulate activated by both pleasant and unpleasant odours, and a more anterior part of the anterior cingulate cortex showing a correlation with the subjective pleasantness ratings of the odours. Thus the results suggest that there is a hedonic map of the sense of smell in brain regions such as the orbitofrontal cortex, and these results have implications for understanding the psychiatric and related problems that follow damage to these brain areas.

Cognitive Modulation of Olfactory Processing

We showed how cognitive, semantic information modulates olfactory representations in the brain by providing a visual word descriptor, cheddar cheese or body odor, during the delivery of a test odor (isovaleric acid with cheddar cheese flavor) and also during the delivery of clean air. Clean air labeled air was used as a control. Subjects rated the affective value of the test odor as significantly more unpleasant when labeled body odor than when labeled cheddar cheese. In an event-related fMRI design, we showed that the rostral anterior cingulate cortex (ACC)/medial orbitofrontal cortex (OFC) was significantly more activated by the test stimulus and by clean air when labeled cheddar cheese than when labeled body odor, and the activations were correlated with the pleasantness ratings. This cognitive modulation was also found for the test odor (but not for the clean air) in the amygdala bilaterally.

Food Reward in the Absence of Taste Receptor Signaling

Food palatability and hedonic value play central roles in nutrient intake. However, postingestive effects can influence food preferences independently of palatability, although the neurobiological bases of such mechanisms remain poorly understood. Of central interest is whether the same brain reward circuitry that is responsive to palatable rewards also encodes metabolic value independently of taste signaling. Here we show that trpm5-/- mice, which lack the cellular machinery required for sweet taste transduction, can develop a robust preference for sucrose solutions based solely on caloric content. Sucrose intake induced dopamine release in the ventral striatum of these sweet-blind mice, a pattern usually associated with receipt of palatable rewards. Furthermore, single neurons in this same ventral striatal region showed increased sensitivity to caloric intake even in the absence of gustatory inputs. Our findings suggest that calorie-rich nutrients can directly influence brain reward circuits that control food intake independently of palatability or functional taste transduction.

The neural mechanisms of gustation: a distributed processing code

Whenever food is placed in the mouth, taste receptors are stimulated. Simultaneously, different types of sensory fibre that monitor several food attributes such as texture, temperature and odour are activated. Here, we evaluate taste and oral somatosensory peripheral transduction mechanisms as well as the multi-sensory integrative functions of the central pathways that support the complex sensations that we usually associate with gustation. On the basis of recent experimental data, we argue that these brain circuits make use of distributed ensemble codes that represent the sensory and post-ingestive properties of tastants.

Taste-related activity in the human dorsolateral prefrontal cortex

Taste remains one of the least-explored human senses. Cortical taste responses were investigated using neuroimaging in 40 subjects tasting a range of different taste stimuli compared to a neutral tasteless control. Activation was found in the anterior insula/frontal opercular taste cortex and caudal orbitofrontal cortex, both areas established as taste cortical areas by neuronal recordings in primates. A novel finding in this study was a highly significant response to taste in the dorsolateral prefrontal cortex. This may reflect an effect of taste on cognitive processing to help optimise or modify behavioural strategies involved in executive control; or it could reflect the engagement of this region in attentional processing by a taste input.

Neural ensemble coding of satiety states.

The motivation to start or terminate a meal involves the continual updating of information on current body status by central gustatory and reward systems. Previous electrophysiological and neuroimaging investigations revealed region-specific decreases in activity as the subjects state transitions from hunger to satiety. By implanting bundles of microelectrodes in the lateral hypothalamus, orbitofrontal cortex, insular cortex, and amygdala of hungry rats that voluntarily eat to satiety, we have measured the behavior of neuronal populations through the different phases of a complete feeding cycle (hunger-satiety-hunger). Our data show that while most satiety-sensitive units preferentially responded to a unique hunger phase within a cycle, neuronal populations integrated single-unit information in order to reflect the animals motivational state across the entire cycle, with higher activity levels during the hunger phases. This distributed population code might constitute a neural mechanism underlying meal initiation under different metabolic states.

Human cortical representation of oral temperature

The temperature of foods and fluids is a major factor that determines their pleasantness and acceptability. Studies of nonhuman primates have shown that many neurons in cortical taste areas receive and process not only chemosensory inputs, but oral thermosensory (temperature) inputs as well. We investigated whether changes in oral temperature activate these areas in humans, or middle or posterior insular cortex, the areas most frequently identified for the encoding of temperature information from the human hand. In the fMRI study we identified areas of activation in response to innocuous, temperature-controlled (cooled and warmed, 5, 20 and 50 degrees C) liquid introduced into the mouth. The oral temperature stimuli activated the insular taste cortex (identified by glucose taste stimuli), a part of the somatosensory cortex, the orbitofrontal cortex, the anterior cingulate cortex, and the ventral striatum. Brain regions where activations correlated with the pleasantness ratings of the oral temperature stimuli included the orbitofrontal cortex and pregenual cingulate cortex. We conclude that a network of taste- and reward-responsive regions of the human brain is also activated by intra-oral thermal stimulation, and that the pleasant subjective states elicited by oral thermal stimuli are correlated with the activations in the orbitofrontal cortex and pregenual cingulate cortex. Thus the pleasantness of oral temperature is represented in brain regions shown in previous studies to represent the pleasantness of the taste and flavour of food. Bringing together these different oral representations in the same brain regions may enable particular combinations to influence the pleasantness of foods.

The insular cortex controls food preferences independently of taste receptor signaling.

The insular cortex (IC) contains the primary sensory cortex for oral chemosensation including gustation, and its integrity is required for appropriate control of feeding behavior. However, it remains unknown whether the role of this brain area in food selection relies on the presence of peripheral taste input. Using multielectrode recordings, we found that the responses of populations of neurons in the IC of freely licking, sweet-blind Trpm5−/− mice are modulated by the rewarding postingestive effects of sucrose. FOS immunoreactivity analyses revealed that these responses are restricted to the dorsal insula. Furthermore, bilateral lesions in this area abolished taste-independent preferences for sucrose that can be conditioned in these Trpm5−/− animals while preserving their ability to detect sucrose. Overall, these findings demonstrate that, even in the absence of peripheral taste input, IC regulates food choices based on postingestive signals.

The Salty and Burning Taste of Capsaicin

The tongue is a kind of funny organ. From a physiological point of view, you can place solutions on the tongue that will be toxic to most any cell, and the tongue will give information, in a hopefully reversible manner, about the solutions chemical composition and whether it should be ingested.