Cortical network and connectivity underlying hedonic olfactory perception

Abstract

Objective. The emotional response to olfactory stimuli implies the activation of a complex cascade of events triggered by structures lying in the limbic system. However, little is known about how this activation is projected up to cerebral cortex and how different cortical areas dynamically interact each other. Approach. In this study, we acquired EEG from human participants performing a passive odor-perception task with odorants conveying positive, neutral and negative valence. A novel methodological pipeline integrating global field power (GFP), independent component analysis (ICA), dipole source localization was applied to estimate effective connectivity in the challenging scenario of single-trial low-synchronized stimulation. Main results. We identified the brain network and the neural paths, elicited at different frequency bands, i.e. θ ( 4 − 7 H z ) , α ( 8 − 12 H z ) and β ( 13 − 30 H z ) , involved in odor valence processing. This brain network includes the orbitofrontal cortex (OFC), the cingulate gyrus (CgG), the superior temporal gyrus (STG), the posterior cingulate cortex/precuneus (PCC/PCu) and the parahippocampal gyrus (PHG). It was analyzed using a time-varying multivariate autoregressive model to resolve time-frequency causal interactions. Specifically, the OFC acts as the main node for odor perception and evaluation of pleasant and unpleasant stimuli, whereas no specific path was observed for a neutral stimulus. Significance. The results introduce new evidences on the role of the OFC during hedonic perception and underpin its specificity during the odor valence assessment. Our findings suggest that, after the odor onset different, bidirectional interactions occur between the OFC and other brain regions associated with emotion recognition/categorization and memory according to the stimulus valence. This outcome unveils how the hedonic olfactory network dynamically changes based on odor valence.

Valence, Arousal, and Gender Effect on Olfactory Cortical Network Connectivity: A Study Using Dynamic Causal Modeling for EEG

“…The EEG data analyzed in this study was already found to carry relevant information about interacting cortical brain areas during the olfactory stimulation [25]. More in detail, in such a previous study, connectivity measures derived from multivariate autoregressive models (MVAR) have confirmed the central role of the OFC in the processing of emotional olfactory stimuli [43], [44].…”

“…The experiment consisted of a single session in which participants performed 3 minutes of initial rest and three blocks of olfactory stimulation. Each block consisted of 1 minute of pre-stimulus rest, 5s of stimulus administration, 1 minute of post-stimulus rest and an average of 15s of self-assessment questionnaire, during which participants scored the stimulus in terms of valence (from -2 to +2 with a step size of 1) and arousal (from +1 to +5 with a step size of 1) according with the Self-Assessment Manikin (SAM) test [57], [25], [58]- [61]. Stimuli were administered by approaching the vials containing the odorant at about 2cm from participant's nostrils.…”

“…On the other hand, effective connectivity is related to the influence that one neural system exerts over another [22]. Among the latter, Granger-Causality based measures [24] have been successfully applied to EEG data to evaluate frequency-specific bidirectional interactions between brain sources [25], as well as between the OB and the PC by combining EEG and electrobulbographic data [26] during olfactory stimulation. However, also other methods are available in the literature for the estimation of effective connectivity [22].…”

Motor Cortex Response to Pleasant Odor Perception and Imagery: The Differential Role of Personality Dimensions and Imagery Ability

“…For instance, hedonic tagging during olfactory perception guides behaviors such as social interaction, food consumption, reward, and emotional reactivity ( Low et al, 2021 ; Faour et al, 2022 ; Han et al, 2022 ). Previous studies investigating brain activation during exposure to pleasant and unpleasant odors reported the presence of a hedonic map with activation of the medial region of the rostral orbitofrontal cortex ( Grabenhorst et al, 2007 ), the posterior part of insula ( Wicker et al, 2003 ), and the anterior cingulate cortex ( Callara et al, 2021 ) after exposure to pleasant odors. Yet, little is known regarding the activation of motor related areas.…”

Odor Pleasantness Modulates Functional Connectivity in the Olfactory Hedonic Processing Network

“…However, deeper insights into olfactory hedonic processing can be drawn via network-based connectivity analyses that complement prior activation studies. In this direction, the handful of olfaction studies employing EEG functional connectivity analysis are focused on limited characterizations of global changes to the connectivity network in response to pleasant and unpleasant stimuli, or without an investigation of the relevant brain regions using graph theoretic metrics [ 24 , 25 ]. Other efforts focused on collateral cognitive processes (not hedonic processing), such as attention to stimuli [ 26 ] or pathological aspects [ 27 ].…”