Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation

Abstract

We used a 2 x 2 factorial design to dissociate regions responding to taste intensity and taste affective valence. Two intensities each of a pleasant and unpleasant taste were presented to subjects during event-related fMRI scanning. The cerebellum, pons, middle insula, and amygdala responded to intensity irrespective of valence. In contrast, valence-specific responses were observed in anterior insula/operculum extending into the orbitofrontal cortex (OFC). The right caudolateral OFC responded preferentially to pleasant compared to unpleasant taste, irrespective of intensity, and the left dorsal anterior insula/operculuar region responded preferentially to unpleasant compared to pleasant tastes equated for intensity. Responses best characterized as an interaction between intensity and pleasantness were also observed in several limbic regions. These findings demonstrate a functional segregation within the human gustatory system. They also show that amygdala activity may be driven by stimulus intensity irrespective of valence, casting doubt upon the notion that the amygdala responds preferentially to negative stimuli.

Altered Insula Response to Taste Stimuli in Individuals Recovered from Restricting-Type Anorexia Nervosa

“…Importantly, only controls, but not recovered AN, showed a positive relationship between self-ratings of pleasantness and the intensity of the signal for sugar in the insula, ventral, and dorsal putamen as well as anterior cingulate cortex. Consistent with these findings Small et al (2001Small et al ( , 2003a found valence-specific responses in the anterior insula/operculum, OFC, and anterior cingulate cortex in healthy subjects. In contrast, amygdala activity was driven by stimulus intensity irrespective of valence.…”

“…In general, the anterior, less differentiated half of the insula receives the majority of projections from the amygdala and thalamic taste centers, making it an ideal site for the formulation of hedonic representations of taste. Consistent with this, anterior portions of the insula have been shown to be differentially activated to the intensity and valence of pleasant and unpleasant tastes (Small et al, 2003a), and are thus important to examine in the eating disordered population.…”

Imaging methodologies and applications for nutrition research: what can functional MRI offer?

“…Although taste stimulation has consistently activated the same brain regions across multiple f MRI studies, including insula and overlaying operculum, the transduction mechanisms remain incompletely characterised. Previous studies reported the primary taste cortex is located within the anterior insula/frontal operculum (13)(14)(15) with secondary projections to the orbitofrontal cortex (OFC) (16) , amygdala (17) , anterior cingulate cortex (ACC) (18) , ventral striatum (19) and dorsolateral prefrontal cortex (20) . O'Doherty et al were the first to investigate the cortical response to pleasant (glucose) and aversive (salt) taste stimuli by assessing stimuli against a tasteless control stimulus (21) .…”

Affective neuroscience of pleasure: reward in humans and animals

“…In humans, neuroimaging studies have found that the affective valence of pleasure may be coded separately from sensation intensity in a network of brain regions (Anderson and Sobel 2003;Gottfried et al 2002;Rolls et al 2003;Small et al 2003). As an example, taste intensity (but not valence) was coded by anterior insula cortex activity (primary gustatory area), while subjective pleasantness was coded by activity in medial orbitofrontal cortex, midinsular cortex, and in the anterior cingulate cortex (de Araujo et al 2003c;Figs.…”