Brain dynamical network analysis of the hedonic odor processing: effective connectivity and integration with peripheral sympathetic correlates

Emotions can be elicited and perceived through different sensory processes. Although research in the affective field has mainly focused on visual and auditory channels, olfaction represents a powerful albeit underestimated channel to investigate physiological and behavioral emotional responses. In this PhD thesis, I have studied the brain cortical correlates of emotional olfactory processing through the analysis of electroencephalographic signal (EEG). In particular, since hedonic olfactory processing arises from the complex integration among hierarchically organized networks, I focus on the application of EEG effective connectivity techniques to investigate the modulatory effect of hedonic odors on the cortico-cortical interactions. Particularly, the thesis builds on three experimental studies that have investigated different aspects of the olfactory-driven emotional neural response through the application of both data-driven techniques, such as Granger-Causality (GC)-derived measures and physiologically-sound computational models such as Dynamic Causal Modeling (DCM). In the first study, combining independent component analysis (ICA) and clustering methods, we have inferred a group-common network of cortical nodes involved in the hedonic olfactory task. Then, I have estimated their dynamic causal interactions by combining the multivariate autoregressive (MVAR) modeling and the application of GC-derived renormalized Partial Directed Coherence (rPDC). The insights provided by this first study have been used as prior knowledge to build the architecture of an olfactory cortical network upon which I have modeled the modulatory effect of odors’ valence through DCM. In particular, I take advantage of the Parametric Empirical Bayes (PEB) framework to infer the average modulatory effect of valence on the group-connectivity, as well as significant interactions with the perceived level of arousal. Moreover, I test for the hypothesis that well-known gender differences in hedonic olfactory processing are reflected in the average group-connectivity. Finally, in the third study, I have investigated an experimental scenario in which contextual hedonic olfactory cues modulate the visual perception of ambiguous faces. In this scenario, we have also investigated whether the presence or absence of a peripheral sympathetic response elicited by the combined visual-olfactory stimulus can affect the neural processing of the emotional stimulus. To this aim, I develop a novel methodological approach integrating sympathetic information provided by electrodermal activity (EDA) into the framework of DCM and PEB. Our results have provided several new insights into brain hedonic olfactory processing. The application of both GC and DCM has shown that the processing of non-neutral olfactory stimuli can result in different connectivity patterns, rather than differences in cortical activation. Specifically, the administration of both pleasant and unpleasant odors has produced significant interactions among cortical regions, whereas the neutral stimulus has not affected connectivity. Furthermore, the application of DCM and PEB has highlighted an interaction of arousal with the processing of unpleasant odors and has corroborated the hypothesis that gender differences in hedonic odor processing are also reflected by changes in brain connectivity. Finally, the novel EEG-EDA approach has revealed a significant effect of sympathetic arousal and odors’ valence on specific ERP components associated with the processing of faces. Particularly, the results have shown interesting modulatory effects targeting the connectivity of the inferior temporal gyrus (ITG) with other key regions already known to be involved in the processing of faces and odors. These dynamics seem to suggest a role the ITG plays as a regulatory region of sympathetic reflexes and physiological arousal. This thesis contributes to a deeper understanding of the physiological processes underlying hedonic olfaction. Moreover, it provides detailed methodological applications of EEG effective connectivity to the scenario of olfactory stimuli. In particular, the presented innovative EEG-EDA approach can be generalized to investigate the effects of peripheral sympathetic responses on brain dynamics in any event-related scenario of affective stimulation.