Cross-modal integration of emotions in the chemical senses

Abstract

Although the brain structures involved in integrating odorant and trigeminal stimuli are well-documented, there is still a need to clarify (1) how emotional response is represented in the human brain during cross-modal interaction between odors and trigeminal stimuli, and (2) whether the degree of congruency between the two types of stimuli influences these emotional responses and their neural processing. These questions were explored combining psychophysics, event-related potentials (ERP) and fMRI in the same group of 17 subjects under a "congruent condition" (intranasal carbon dioxide mixed with the smell of orange, a combination found in soda drinks, for example), and an "incongruent condition" (intranasal carbon dioxide mixed with the smell of rose, a combination not encountered in everyday life). Responses to the 3 constituent stimuli (carbon dioxide, orange, and rose) were also measured. Hedonic and intensity ratings were collected for all stimulations. The congruent bimodal stimulus was rated as more pleasant than the incongruent. This behavioral effect was associated with enhanced neural activity in the hippocampus and anterior cingulate gyrus, indicating that these brain areas mediate reactivation of pleasant and congruent olfactory-trigeminal associations.

Keywords: congruency; emotion; fMRI; olfaction; trigeminal.

Figure 1

Experimental design, protocol and congruency ratings. (A) The experimental design comprised 5 conditions (3 individual components and 2 mixtures). (B) Schematic representation of the experimental protocol used during the fMRI sessions. (C) 2 × 2 design used in fMRI, behavioral and EEG analyses. (D) Congruency ratings: the [CO₂+Orange] mixture was rated as significantly more congruent than [CO₂+Rose] in “pair rating” and “mixture rating” paradigms. Bars represent s.e.m. ^*p < 0.05.

Figure 2

Brain activation and perceptual ratings. (A) Brain activation and contrast estimates in response to the congruent mixture (vs. air) vs. the incongruent mixture (vs. air): responses were observed in anterior cingulate cortex (CING, p < 0.05 SVC). (B) Brain activation and contrast estimates in response to the congruent mixture (vs. its components) vs. the incongruent mixture (vs. its components): responses were observed in the hippocampus (HIP, p < 0.05 SVC) and anterior cingulate cortex (CING, p < 0.05 SVC). (C) Differential ratings, showing pleasantness and intensity ratings for the congruent and incongruent mixtures vs. their individual components (Compo). ^*p < 0.05; ns = non-significant difference at the 0.05 threshold. Bars represent s.e.m.

Figure 3

EEG measurements. (A) Grand average of chemosensory event-related potentials averaged across all electrodes and subjects for the unimodal and bimodal conditions, showing the N1 and P2 components. (B) Chemosensory event-related potentials for the 4 experimental conditions: bimodal congruent mixture (CO₂Orange), bimodal incongruent mixture (CO₂Rose), unimodal congruent components (CO₂+Orange) and unimodal congruent components (CO₂+Rose) in Fz, Cz, and Pz electrode sites.