Evidence for an Integrated Oral Sensory Module in the Human Anterior Ventral Insula

Abstract

Taste, which is almost always accompanied by other oral sensations, serves to identify potential nutrients and toxins. The present study was designed to determine the influence of sensory modality (chemesthetic vs. gustatory) and physiological significance (potentially nutritive vs. potentially harmful) on insular response to oral stimulation. Sixteen subjects underwent functional magnetic resonance imaging scanning while receiving 2 potentially nutritive solutions (sucrose and NaCl), 2 potentially harmful solutions (quinine and capsaicin, a chemesthetic stimulus), and a tasteless control solution. We identified a region of anterior ventral insula that responded to oral stimulation irrespective of modality or physiological significance. However, when subjects tasted a potentially nutritive stimulus, the connectivity between the insula and a feeding network including the hypothalamus, ventral pallidum, and striatum was greater than when tasting a potentially harmful stimulus. No differential connectivity was observed as a function of modality (gustatory vs. chemesthetic). These results support the existence of an integrated supramodal flavor system in the anterior ventral insula that preferentially communicates with the circuits guiding feeding when the flavor is potentially nutritive.