Brain Responses to Emotional Stimuli During Breath Holding and Hypoxia: An Approach Based on the Independent Component Analysis

Voluntary breath holding represents a physiological model of hypoxia. It consists of two phases of oxygen saturation dynamics: an initial slow decrease (normoxic phase) followed by a rapid drop (hypoxic phase) during which transitory neurological symptoms as well as slight impairment of integrated cerebral functions, such as emotional processing, can occur. This study investigated how breath holding affects emotional processing. To this aim we characterized the modulation of event-related potentials (ERPs) evoked by emotional-laden pictures as a function of breath holding time course. We recorded ERPs during free breathing and breath holding performed in air by elite apnea divers. We modeled brain responses during free breathing with four independent components distributed over different brain areas derived by an approach based on the independent component analysis (ICASSO). We described ERP changes during breath holding by estimating amplitude scaling and time shifting of the same components (component adaptation analysis). Component 1 included the main EEG features of emotional processing, had a posterior localization and did not change during breath holding; component 2, localized over temporo-frontal regions, was present only in unpleasant stimuli responses and decreased during breath holding, with no differences between breath holding phases; component 3, localized on the fronto-central midline regions, showed phase-independent breath holding decreases; component 4, quite widespread but with frontal prevalence, decreased in parallel with the hypoxic trend. The spatial localization of these components was compatible with a set of processing modules that affects the automatic and intentional controls of attention. The reduction of unpleasant-related ERP components suggests that the evaluation of aversive and/or possibly dangerous situations might be altered during breath holding.