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Abstract:
The transmission of sensory information facilitates the communication between body and brain. One specialized brain region, the insular cortex (IC), encodes sensory information related to interoceptive and gustatory processing. In an effort to topographically compare functional representations with the anatomically distinct subregions of the IC, a series of experiments were conducted using fMRI and electrophysiology in macaque monkeys, and to a lesser extent fMRI in humans, whereby both interoceptive and gustatory pathways were stimulated using multimodal stimuli. The gustatory pathway was stimulated using specific sets of taste stimuli, including sweet, sour and salty tastants, applied to the tongue at high- and low-intensity concentrations in macaques and humans. While variability was observed in the localization of specific regions of interest across individuals and taste qualities, a consistent pattern was observed where two anatomically separate regions responded to taste stimulation across the IC in both species. One region was consistently localized to the anteroposterior mid-dorsal fundus of the IC. Another more variable activation occurred in the most anterior aspect of the fundus, with a clear separation of several millimeters from the middle representation. Further stimulations of the interoceptive pathway using transcutaneous stimulation of the auricular branch of the vagus nerve (tVNS), rectal distention (RD), and local skin temperature modulation in macaque monkeys disclosed a particular functional organization. Thermal stimulation of the limbs (hand and foot) consistently activated a region posterior to the middle taste representation. Both RD and tVNS variably activated a smaller region near the taste representation and another region in the ventral and anterior aspect of the IC, a region that contains von Economo neurons and that has been related to a network of high-order cognitive functions and top-down influence on the autonomic nervous system. Electrophysiological recordings throughout the entire anteroposterior extent of the insula largely confirmed this topography. These non- or minimally-invasive stimulations of the primary interoceptive cortex provide the first multimodal mapping of interoceptive modalities in the IC. This mapping and its future elaborations are of paramount importance for our appreciation of the neurobiological substrate underlying the embodiment of subjective feelings and the psychosomatic relation between brain and bodily states during high-order emotional and cognitive functions.
