The pathways of interoceptive awareness

Abstract

A network of cortical brain regions, including the insula and anterior cingulate cortex (ACC), has been proposed as the critical and sole substrate for interoceptive awareness. Combining lesion and pharmacological approaches in humans, we found that the insula and ACC were not critical for awareness of heartbeat sensations. Instead, this awareness was mediated by both somatosensory afferents from the skin and a network that included the insula and ACC. Together, these pathways enable the core human experience of the cardiovascular state of the body.

Figure 1

Schematic representing possible pathways of interoceptive awareness. Two possible interoceptive awareness “pathways” are envisioned: one involving visceral afferents projecting to the insula (green arrow), and another involving somatosensory skin afferents (cyan arrow). Several alternative hypotheses can be proposed: interoceptive awareness is only mediated by the insula pathway (H1; standard hypothesis); interoceptive awareness is only mediated by the somatosensory pathway (H2); interoceptive awareness is independently mediated by each pathway (H3); interoceptive awareness is dependent on the simultaneous action of both pathways (H4); finally, interoceptive awareness could be dependent on other pathways (H5). If H1 is true, then only bilateral damage to the insula pathway should abolish interoceptive awareness. If H2 is true, then only disrupting the somatosensory pathway should abolish interoceptive awareness. If H3 is true, then disruption of either pathway should not abolish interoceptive awareness but disruption of both should. If H4 is true, then disrupting either pathway should abolish interoceptive awareness. If H5 is true, disruption of both pathways should not abolish interoceptive awareness. Results are in support of H3 (dashed outline). + indicates interoceptive awareness present, − indicates interoceptive awareness absent. See text for details.

Figure 2

Brain damage in patient Roger. Top: extent of damage (black) on MRI views of lateral (upper left and right), ventral (middle) and mesial (lower left and right) cerebrum. Bottom: Axial (a–d) and saggital (1–4) slices (cf top lines). Ins = insula.

Figure 3

Heart rate response and online subjective dial ratings of interoceptive awareness changes induced by isoproterenol. (a) Roger and eleven healthy age-matched male comparison participants exhibited equivalent dose-dependent heart rate increases. (b) Time course of heart rate response and dial ratings. Roger and the healthy participants appropriately demonstrated dose-dependent changes in interoceptive awareness. Bolus infusions occurred at time zero. (c) Overlap map showing the region of maximal heartbeat sensation, corresponding to the area of topical anesthetic application. (d) Time course of heart rate response and dial ratings after anesthetic application. Roger no longer demonstrated appropriate changes in interoceptive awareness, even at the two highest doses. Comparisons' interoceptive awareness was unaffected. All comparison data depict means. Error bars = SE. See supplementary material for additional results.