Viewing images of foods evokes taste quality-specific activity in gustatory insular cortex

Jason A Avery, Alexander G Liu, John E Ingeholm, Stephen J Gotts, Alex Martin, Jason A Avery, Alexander G Liu, John E Ingeholm, Stephen J Gotts, Alex Martin

Abstract

Previous studies have shown that the conceptual representation of food involves brain regions associated with taste perception. The specificity of this response, however, is unknown. Does viewing pictures of food produce a general, nonspecific response in taste-sensitive regions of the brain? Or is the response specific for how a particular food tastes? Building on recent findings that specific tastes can be decoded from taste-sensitive regions of insular cortex, we asked whether viewing pictures of foods associated with a specific taste (e.g., sweet, salty, and sour) can also be decoded from these same regions, and if so, are the patterns of neural activity elicited by the pictures and their associated tastes similar? Using ultrahigh-resolution functional magnetic resonance imaging at high magnetic field strength (7-Tesla), we were able to decode specific tastes delivered during scanning, as well as the specific taste category associated with food pictures within the dorsal mid-insula, a primary taste responsive region of brain. Thus, merely viewing food pictures triggers an automatic retrieval of specific taste quality information associated with the depicted foods, within gustatory cortex. However, the patterns of activity elicited by pictures and their associated tastes were unrelated, thus suggesting a clear neural distinction between inferred and directly experienced sensory events. These data show how higher-order inferences derived from stimuli in one modality (i.e., vision) can be represented in brain regions typically thought to represent only low-level information about a different modality (i.e., taste).

Trial registration: ClinicalTrials.gov NCT00001360.

Keywords: MVPA; fMRI; insula; multimodal; taste.

Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Experimental design. (A) An overview of the experimental session, during which participants performed food pictures and taste perception fMRI tasks, separated by two nonscanning behavioral rating tasks. (B and C) During the food pictures fMRI task, subjects viewed pictures of a variety of food and nonfood objects within randomly ordered presentation blocks during scanning. Foods were categorized into predominantly sweet, sour, and salty foods, as well as nonfood familiar objects, selected on the basis of a series of prior experiments with a large online sample of participants. (D) During the taste perception fMRI task, participants received sweet, sour, salty, and neutral tastant solutions, delivered in randomly ordered stimulus blocks, during scanning.
Fig. 2.
Fig. 2.
Bilateral regions of the ventral anterior and dorsal mid-insula (MI) are responsive to taste perception and viewing pictures of food. Univariate analysis results from both imaging tasks. (A) All tastes (sweet, sour, and salty) vs. the neutral tastant activated bilateral regions of the dorsal MI, as well as left ventral anterior insula (vAI) and right dorsal anterior insula (dAI). (B) All food vs. object pictures activated bilateral MI and ventral anterior insula, as well as left OFC (not pictured). (C) An overlap of the maps from A and B revealed bilateral ventral anterior and MI regions coactivated by food pictures and taste.
Fig. 3.
Fig. 3.
MVPAs reliably classify taste quality and food picture category within bilateral regions of the dorsal MI. Taste-responsive regions of the bilateral insula, which were identified using the same taste paradigm within an independent dataset (12), were used as regions of interest for multivariate classification analyses performed on both imaging tasks. Within the bilateral dorsal MI, we were able to reliably classify both taste quality and food picture category, whereas we could classify only tastes within dAI. We could not reliably cross-classify food pictures by training on tastes, or vice versa.
Fig. 4.
Fig. 4.
MVPAs classify food pictures according to taste category within brain regions involved in taste perception, arousal, and reward.Several regions of the brain were identified using a multivariate searchlight analysis trained to discriminate between pictures of sweet, salty, and sour foods. This included regions involved in processing the sensory and affective components of food, including bilateral regions of the dorsal mid-insula and ventral anterior insula, as well as the bilateral postcentral gyrus, the bilateral OFC, inferior frontal gyrus (IFG), and the left amygdala.
Fig. 5.
Fig. 5.
A common set of brain regions supporting information about taste quality and food picture category. A conjunction of multivariate searchlight maps performed on both taste perception and food pictures tasks identifies a set of regions which reliably discriminate between both taste quality and food picture category. This set of regions included sensory cortical areas within the mid-insular cortex and somatosensory cortex, as well as regions of the ventral occipitotemporal object processing stream.

Source: PubMed

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