Respiration Modulates Olfactory Memory Consolidation in Humans

Abstract

In mammals respiratory-locked hippocampal rhythms are implicated in the scaffolding and transfer of information between sensory and memory networks. These oscillations are entrained by nasal respiration and driven by the olfactory bulb. They then travel to the piriform cortex where they propagate further downstream to the hippocampus and modulate neural processes critical for memory formation. In humans, bypassing nasal airflow through mouth-breathing abolishes these rhythms and impacts encoding as well as recognition processes thereby reducing memory performance. It has been hypothesized that similar behavior should be observed for the consolidation process, the stage between encoding and recognition, were memory is reactivated and strengthened. However, direct evidence for such an effect is lacking in human and nonhuman animals. Here we tested this hypothesis by examining the effect of respiration on consolidation of episodic odor memory. In two separate sessions, female and male participants encoded odors followed by a 1 h awake resting consolidation phase where they either breathed solely through their nose or mouth. Immediately after the consolidation phase, memory for odors was tested. Recognition memory significantly increased during nasal respiration compared with mouth respiration during consolidation. These results provide the first evidence that respiration directly impacts consolidation of episodic events, and lends further support to the notion that core cognitive functions are modulated by the respiratory cycle.SIGNIFICANCE STATEMENT Memories pass through three main stages in their development: encoding, consolidation, and retrieval. Growing evidence from animal and human studies suggests that respiration plays an important role in the behavioral and neural mechanisms associated with encoding and recognition. Specifically nasal, but not mouth, respiration entrains neural oscillations that enhance encoding and recognition processes. We demonstrate that respiration also affects the consolidation stage. Breathing through the nose compared with the mouth during consolidation enhances recognition memory. This demonstrates, first, that nasal respiration is important during the critical period were memories are reactivated and strengthened. Second, it suggests that the neural mechanisms responsible may emerge from nasal respiration.

Keywords: consolidation; episodic; hippocampus; memory; odor; respiration.