Interoceptive accuracy and its impact on neuronal responses to olfactory stimulation in the insular cortex

• Published in: Human brain mapping 2020-08, Vol.41 (11), p.2898-2908
• Main Authors: Koeppel, Carina J., Ruser, Paul, Kitzler, Hagen, Hummel, Thomas, Croy, Ilona
• Format: Article
• Language: English
• Subjects: Accuracy; Chemoreception; Coffee; Cortex (insular); exteroception; Functional magnetic resonance imaging; Heart; Information processing; insular cortex; interoception; interoceptive accuracy; Odor; Odors; Olfaction; Olfactory system; Sensory integration; Sensory stimulation; Smell
• ISSN: 1065-9471; 1097-0193
• DOI: 10.1002/hbm.24985

The insular cortex plays a key role in the integration of multimodal information and in interoceptive and exteroceptive processing. For instance, neurons in the central dorsal insula that are active during interoceptive tasks, also show an adaptation to gustatory stimulation. We tested the link between interoception and exteroception for the olfactory system (i.e., the second domain of chemosensation). In a sample of 31 participants, olfactory function was assessed in a two dimensional approach while the Heartbeat Perception Task served as a measurement for cardiac interoceptive accuracy. Subsequent fMRI sessions were performed on a 3‐Tesla MR scanner containing 12–15 olfactory stimulation trials with a mildly pleasant food‐related odor (coffee). Persons scoring high in the cardiac interoceptive accuracy task presented stronger smelling abilities as well as enhanced BOLD responses following olfactory stimulation. The olfactory stimulation triggered enhanced insular activation patterns in the central dorsal insular cortex. Consistent with prior findings on the coherence of gustatory and interoceptive processing in the central dorsal insula, these results base the insula as a common region for the integration of interoception and exteroception. We propose an explanatory model of how exteroception triggers the integration of intero‐ and exteroceptive sensations in the central dorsal insular cortex. The integration of intero‐ and exteroceptive input is crucial for detecting the salience of surrounding stimuli. Participants with high cardiac interoceptive accuracy present stronger central‐dorsal insular activation patterns during olfactory stimulation. An explanatory model is proposed focusing on an exteroceptive trigger for the multimodal integration in the central‐dorsal insula.