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.

Respiration competes with theta for modulating parietal cortex neurons

“…Such a widespread influence could potentially relate to the effects of respiration over emotional states and cognitive functions [30][31][32][33][34]. Noteworthy, it has been increasingly recognized that nasal respiration modulates performance in cognitive tasks [35][36][37], including non-olfactory ones [38].…”

The Respiratory Modulation of Memory

“…Although brain activity was not monitored in this study, Arshamian et al (2018) suggest that a specific type of hippocampal oscillations named sharp-wave ripples (SWRs) are involved in their results. These highly synchronized fast oscillations occur in the hippocampal formation during sleep or awake rest periods and are thought to be involved in the replay of past events.…”

“…In mice, the respiratory phase modulates the occurrence of SWRs (Liu et al, 2017), but the effect disappears if the olfactory bulb is inhibited (via bilateral injection of viral vectors), suggesting it depends on the olfactory reafferent rhythm. Because breathing through the mouth does not activate the olfactory reafferent rhythm in humans, Arshamian et al (2018) argue that the respiratory modulation of SWRs would be abolished during mouth breathing and that this reduced occurrence of SWRs leads to decreased olfactory memory consolidation.…”

“…Altogether, through its cross-frequency coupling with the delta waves, the olfactory reafferent rhythm could modulate both the occurrence of SWRs and the hippocampo-cortical dialogue involved in memory consolidation (Buzsáki, 1996). Therefore, reductions in delta-wave modulation during mouth breathing might contribute to the reduced memory consolidation in the experiments by Arshamian et al (2018).…”

“…Beyond the well documented olfactory reafferent rhythm (Tort et al, 2018), a recent study by Karalis and Sirota (2018) suggests the existence of a respiratory modulation pathway that is independent of the breathing mode and might also modulate memory consolidation. Like Arshamian et al (2018); Karalis and Sirota (2018) investigated the effect of breathing on memory consolidation, but using a fear conditioning paradigm in mice. They measured the respiratory entrainment of neural activity in several brain regions, including the mPFC and the hippocampus, through multiple single-neuron recordings.…”