EEG slow oscillations and overnight spatial navigational memory performance in CPAP-treated obstructive sleep apnea

Abstract

Obstructive sleep apnea (OSA) exerts pathogenic effects through a combination of sleep fragmentation (SF) and intermittent hypoxia (IH). The mechanisms through which sleep disruption impacts memory might arise by investigating disruption of specific sleep stages and, when such disruption occurs through OSA, by evaluating the individual contributions of SF and IH. Given that region-specific EEG slow activity during non-REM sleep has been associated with overnight declarative, motor, and spatial memory formation, we investigated the effects of disrupting slow wave sleep (SWS) on a virtual maze navigation task. Thirty-three participants (24 male, 56 years old [range 28-68 years] with OSA (baseline AHI4%>20/h) who were habitually well-treated and adherent to continuous positive airway pressure (CPAP) completed 3 timed trials on a 3D spatial maze before and after polysomnographically (PSG) recorded sleep. We restricted CPAP withdrawal to SWS through real-time monitoring of the PSG under three conditions: (1) stable SWS on therapeutic CPAP, (2) SWS-CPAP withdrawal containing SF and IH, and (3) SWS-CPAP withdrawal with supplemental oxygen containing SF with reduced IH. SWS-specific CPAP withdrawal (with or without supplemental oxygen) did not significantly impact EEG slow oscillation or spatial navigational memory despite effectively reducing %SWS and SWS bout length. Greater regional EEG slow oscillation (0.6-1 Hz), but not delta (1-4 Hz) activity, was associated with improvements in overnight memory during stable SWS in the CPAP condition. These observations suggest that slow oscillations may be important for overnight memory processing, and sleep disruptions of sufficient magnitude to reduce slow oscillations may be required to capture demonstrable change in spatial navigation performance.

Keywords: intermittent hypoxia; positive airway pressure; sleep fragmentation; slow oscillations; spatial navigation.

Figure 1.

Slow wave sleep (SWS) bout length (A) and as a percentage of TST (B).

Figure 2.

EEG topoplots of Delta (1–4 Hz) (top) and SOA (0.6–1 Hz) (bottom) power in each of the three conditions during SWS.

Figure 3.

PVT mean reaction time (A) and lapses (B).

Figure 4.

Maze CT by trial (A) and overnight change (B).

Figure 5.

Correlation topoplots show greater regional SOA (0.6–1 Hz) during SWS is associated with improvements in overnight spatial memory performance during the CPAP-uninterrupted SWS (left) and SWS OSA (right) conditions. Electrodes highlighted in white indicate a significant association p < .05, and an asterisk indicates a significant association after adjustment, p < .003.