Corticolimbic structures activation during preparation and execution of respiratory manoeuvres in voluntary olfactory sampling: An intracranial EEG study

Volitional respiratory manoeuvres such as sniffing and apnoea play a key role in the active olfactory exploration of the environment. Their impairment by neurodegenerative processes could thus impair olfactory abilities with the ensuing impact on quality of life. Functional brain imaging studies have identified brain networks engaged in sniffing and voluntary apnoea, comprising the primary motor and somatosensory cortices, the insula, the anterior cingulate cortex and the amygdala. The temporal organization and the oscillatory activities of these networks are not known. To elucidate these aspects, we recorded intracranial electroencephalograms in six patients during voluntary sniffs and short apnoeas (12 s). The preparation phase of both manoeuvres involved increased alpha and theta activity in the posterior insula, amygdala and temporal regions, with a specific preparatory activity in the parahippocampus for the short apnoeas and the hippocampus for sniff. Subsequently, it narrowed to the superior and median temporal areas, immediately after the manoeuvres. During short apnoeas, a particular dynamic was observed, consisting of a rapid decline in alpha and theta activity followed by a slow recovery and increase. Volitional respiratory manoeuvres involved in olfactory control involve corticolimbic structures in both a preparatory and executive manner. Further studies are needed to determine whether diseases altering deep brain structures can disrupt these mechanisms and if such disruption contributes to the corresponding olfactory deficits. KEY POINTS: Both sniff manoeuvres and short apnoeas are associated with oscillatory activity predominantly in low-frequency bands (alpha and theta). Preparation of sniff manoeuvres and short apnoeas involve activities in low-frequency bands in the posterior insula and temporal regions that extend to amygdala during the execution of both manoeuvres. During short apnoeas, activities in low-frequency bands initially decline before continuously increasing until the apnoeas end.