Effects of obstructive sleep apnea on human spatial navigational memory processing in cognitively normal older individuals

Abstract

Study objectives: Obstructive sleep apnea (OSA) prevalence increases with age, but whether OSA-related sleep disruption could interrupt the processing of previously encoded wake information thought to normally occur during sleep in cognitively normal older adults remains unknown.

Methods: Fifty-two older (age = 66.9 ± 7.7 years, 56% female), community-dwelling, cognitively normal adults explored a 3-D maze environment and then performed 3 timed trials before (evening) and after (morning) sleep recorded with polysomnography with a 20-minute morning psychomotor vigilance test.

Results: Twenty-two (22) participants had untreated OSA [apnea-hypopnea index (AHI4%) ≥ 5 events/h] where severity was mild on average [median (interquartile range); AHI4% = 11.0 (20.7) events/h] and 30 participants had an AHI4% < 5 events/h. No significant differences were observed in overnight percent change in completion time or in the pattern of evening presleep maze performance. However, during the morning postsleep trials, there was a significant interaction between OSA group and morning trial number such that participants with OSA performed worse on average with each subsequent morning trial, whereas those without OSA showed improvements. There were no significant differences in morning psychomotor vigilance test performance, suggesting that vigilance is unlikely to account for this difference in morning maze performance. Increasing relative frontal slow wave activity was associated with better overnight maze performance improvement in participants with OSA (r = .51, P = .02) but not in those without OSA, and no differences in slow wave activity were observed between groups.

Conclusions: OSA alters morning performance in spatial navigation independent of a deleterious effect on morning vigilance or evening navigation performance. Relative frontal slow wave activity is associated with overnight performance change in older participants with OSA, but not those without.

Keywords: Alzheimer disease; EEG; SWA; elderly; learning.

Figure 1. Sleep fragmentation assessed using cumulative duration probability distribution shows stage-specific differences according to OSA diagnosis.

Survival curves (cumulative probability distributions) of stage-specific sleep runs in non-OSA (blue) and OSA (orange). The survival curves showed a significant shift toward less continuous REM (A) and NREM 2 (C) sleep bouts in OSA (orange) compared with non-OSA (blue), and more continuous SWS (D) in OSA compared to participants without OSA (***P < .00001, **P < .0001, *P < .05, n.s. = not significant, log-rank test). No significant difference between groups was observed in the survival curves for NREM 1 (B). NREM = non–rapid-eye movement, OSA = obstructive sleep apnea, REM = rapid eye movement, SWS = slow wave sleep.

Figure 2. Overnight change in spatial navigation completion time is not different according to OSA diagnosis.

Overnight change in maze completion time was not statistically different between older participants with (orange) and without (blue) OSA. Crossbars represent mean and standard error values. n.s. = not significant, OSA = obstructive sleep apnea.

Figure 3. Spatial navigation completion time changes across trials.

There were no significant differences in presleep maze completion times (trials 1–3) or postsleep maze completion times (trials 4–6) between those with (orange) and without (blue) OSA. However, there was a significant interaction between OSA group and morning postsleep trial number (2-way repeated measures analysis of variance). n.s. = not significant, *P < .05, OSA = obstructive sleep apnea.

Figure 4. There were no significant differences in PVT reaction time or lapses between participants with and without OSA.

There were no significant differences between participants with OSA (orange) and participants without OSA (blue) for mean reaction times (A) and lapses (reaction time > 500 ms) (B) during the morning PVT. Box and whiskers represent median and interquartile range values. n.s. = not significant, OSA = obstructive sleep apnea, PVT = psychomotor vigilance testing.

Figure 5. More self-reported sleepiness in participants with OSA after 20-minute psychomotor vigilance testing.

Participants with OSA (orange) reported significantly greater sleepiness after PVT (B) but not before PVT (A) than participants without OSA (blue). Box and whiskers represent median and interquartile range values. n.s. = not significant, *P < .05, OSA = obstructive sleep apnea, PVT = psychomotor vigilance testing.

Figure 6. Greater SWA in OSA is associated with better overnight maze completion time performance.

Greater relative SWA (0.5–4 Hz) during NREM sleep at frontal electroencephalogram positively correlates with better overnight maze performance improvements in participants with OSA (r = .51, P = .02) but not in those without OSA. A negative value for overnight change indicates slower, on average, postsleep maze completion times compared to presleep completion times. NREM = non–rapid eye movement, OSA = obstructive sleep apnea, SWA = slow wave activity.