Respiration-phased switching between sensory inputs and top-down inputs in the olfactory cortex

Olfactory perception depends on respiration phases: olfactory cortex processes external odor signals during inhalation whereas it is isolated from the external odor world during exhalation. Olfactory cortex pyramidal cells receive the sensory signals via bottom-up pathways terminating on superficial layer (SL) dendrites while they receive top-down inputs on deep layer (DL) dendrites. Here we asked whether olfactory cortex pyramidal cells spontaneously change the action modes of receiving olfactory sensory inputs and receiving top-down inputs in relation to respiration phases. Current source density analysis of local field potentials recorded in three different olfactory cortex areas of waking immobile rats revealed β- and γ-range fast oscillatory current sinks and a slow current sink in the SL during inhalation, whereas it showed β- and γ-range fast oscillatory current sinks and a slow current sink in the DL during exhalation. Sensory deprivation experiments showed that inhalation-phased olfactory sensory inputs drove the inhalation-phased fast oscillatory potentials in the SL but they drove neither the inhalation-phased slow current sink in the SL nor the exhalation-phased slow current sink in the DL. The results indicate that independent of inhalation-phased olfactory sensory inputs, olfactory cortex pyramidal cells spontaneously generate a slow depolarization in the SL dendrites during inhalation, which may selectively boost the concomitant olfactory sensory inputs to elicit spike outputs. In addition, the pyramidal cells spontaneously generate slow depolarization in the DL dendrites during exhalation, which may assist top-down inputs to elicit spike outputs. We thus hypothesize that the olfactory cortical areas coordinately perform inhalation/exhalation-phased switching of input biasing: inhalation phase is the time window for external odor signals that arrive in the SL dendrites, whereas exhalation phase is assigned to boost top-down signals to the DL dendrites that originate in higher brain centers.