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.

Figure 1.

Schematic of experimental paradigm. The experiment consisted of two separate sessions, each including an encoding, a consolidation, and a recognition phase. In the encoding phase, participants were presented with six familiar (e.g., strawberry) and six unfamiliar (e.g., 1-butanol) odors one at a time and asked to remember them. The odors familiarity was predefined and a new set of odors were used in each session. After the encoding phase, participants rested passively without sleeping (consolidation phase) for 1 h during which they either breathed through their nose (nasal consolidation) or mouth (mouth consolidation). Next, during the odor recognition phase, participants were once again presented with the odors from the encoding phase but this time intermixed with 12 new odors (6 familiar and 6 unfamiliar odors). For each odor, participants made a recognition judgment if the odor was new or old. Next participants rated odor intensity, pleasantness, familiarity, and nameability, as well as trying to identify the odor. During both encoding and recognition, nasal airflow was monitored by a nasal cannula, which enabled measurement of sniff parameters during odor presentation.

Figure 2.

Recognition memory (d′) as function of nasal and mouth respiration during consolidation. Violin plot for recognition memory using the sensitivity index d′ after nasal and mouth consolidation sessions. The d′ was calculated for the familiar and unfamiliar odors separately but for simplicity are collapsed here. The boxes indicate the 75th (upper horizontal line), mean + SEM (black bold horizontal line), median (white dot), and the 25th (lower horizontal line), percentiles of the distribution. The upper whiskers indicate the maximum value of the variable located within a distance of 1.5 times the interquartile range above the 75th percentile. The lower whiskers indicate the corresponding distance to the 25th percentile value. Surrounding the boxes (shaded area) on each side is a rotated kernel density plot, which is comparable to a histogram with infinitely small bin sizes.

Figure 3.

Sniff parameters during odor encoding and recognition across sessions. A, Average continuous sniff response during odor encoding across sessions with 95% confidence interval (CI). Gray volume of the 95% CI indicates the area were the nasal consolidation (light blue) and mouth consolidation (light orange) sniffing parameters overlap. B, C, AUC and the FWHM with corresponding 95% CI during odor encoding across sessions. D, Average continuous sniff response during odor recognition sessions with 95% CI. E, F, The AUC and the FWHM with corresponding 95% CI during odor recognition across sessions. G, H, Data from one participant displaying 12 s of a 10-samples moving average continuous respiration (6 s before odor presentation and 6 s after) during both encoding and recognition for nose and mouth respiration. The unit used is in proportion (∝) pressure change, measured in arbitrary units (AU).

Figure 4.

Response bias (c) as function of nasal and mouth respiration during consolidation. Violin plots for response bias c for nasal and mouth consolidation conditions. The c was calculated for the familiar and unfamiliar odors separately but here are collapsed for clarity. For a fuller description of figure markings, see Figure 2.

Figure 5.

Attentional control as function of respiration route. A, B, Violin plots for the SART and the color–word Stroop task measuring selective attention. For description of figure markings, see Figure 2.