Chapter 16 - Reduction of nocturnal slow-wave activity affects daytime vigilance lapses and memory encoding but not reaction time or implicit learning

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Abstract

Total sleep deprivation in healthy subjects has a profound effect on the performance on tasks measuring sustained attention or vigilance. We here report how a selective disruption of deep sleep only, that is, selective slow-wave activity (SWA) reduction, affects the performance of healthy well-sleeping subjects on several tasks: a “simple” and a “complex” vigilance task, a declarative learning task, and an implicit learning task despite unchanged duration of sleep.

We used automated electroencephalogram (EEG) dependent acoustic feedback aimed at selective interference with—and reduction of—SWA. In a within-subject repeated measures crossover design, performance on the tasks was assessed in 13 elderly adults without sleep complaints after either SWA-reduction or after normal sleep.

The number of vigilance lapses increased as a result of SWA reduction, irrespective of the type of vigilance task. Recognition on the declarative memory task was also affected by SWA reduction, associated with a decreased activation of the right hippocampus on encoding (measured with fMRI) suggesting a weaker memory trace. SWA reduction, however, did not affect reaction time on either of the vigilance tasks or implicit memory task performance.

These findings suggest a specific role of slow oscillations in the subsequent daytime ability to maintain sustained attention and to encode novel declarative information but not to maintain response speed or to build implicit memories. Of particular interest is that selective SWA reduction can mimic some of the effects of total sleep deprivation, while not affecting sleep duration.

Introduction

Disruption of sleep affects daytime cognitive functioning, as borne out by a rich literature on the subject. Among those functions are vigilance and memory. Acute sleep deprivation in healthy subjects leads to reduced vigilance, as shown by a higher number of lapses, that is, late or absent responses to the stimuli (Dinges et al., 1997, Drummond et al., 2005, Van Dongen et al., 2004) and also leads to a reduced capacity for learning new declarative material (Yoo et al., 2007). These studies use total sleep deprivation to investigate the effect of sleep loss. The results do not allow to (1) judge which sleep phase or sleep parameters are most strongly involved in the effects of sleep deprivation or (2) show how different forms of memory are affected by sleep disruption.

We here aimed to investigate the effects of a specific sleep disruption, targeting deep sleep, without the confound of sleep deprivation, on different memory tasks to study their differential sensitivity.

To do so, we exposed healthy volunteers without sleep complaints to two full nights of selective slow-wave activity (SWA) reduction (Arima et al., 2001, Drewes et al., 2000, Landsness et al., 2009, Van Der Werf et al., 2009) prior to one of two cognitive testing sessions. The same volunteers were allowed two nights of normal sleep prior to the other testing session. The SWA-reduction method selectively attenuates SWA and increases alpha power. Reduced SWA and increased alpha power have both been related to the severity of subjective sleep complaints of primary insomnia patients (Krystal et al., 2002). As such, the selective SWA reduction may represent a more “ecologically valid” model of the attenuation of slow-wave sleep in primary insomnia than the frequently applied total sleep deprivation model. In spite of the fact that insomnia is the most frequent sleep disorder and a frequent complaint in psychological practice, only a few studies have quantitatively addressed the daytime behavioral, cognitive, and brain abnormalities of the condition (Altena, Van Der Werf, Sanz-Arigita, et al., 2008, Altena, Van Der Werf, Strijers and Van Someren, 2008). Virtually, no study has evaluated the validity of experimental models for daytime complaints of insomnia, which are much needed in order to accelerate progress in our understanding of this condition.

We measured, both after normal sleep and after selective SWA interference: (a) vigilance using two adaptations of the psychomotor vigilance task (PVT), that is, a “simple” vigilance task requiring the subject to respond to an unpredictably occurring target stimulus on a computer screen (no other stimulus was presented throughout the task) and a “complex” vigilance task, requiring the subject to respond to one of two occurring stimuli; (b) declarative memory using encoding of novel pictures, followed by a recognition trial; and (c) implicit memory by requiring subjects to perform a sequence of button presses, which contained, unbeknownst to the subject, a hidden fixed sequence. Improved performance on this task is shown by a faster reaction time on the fixed sequence relative to the random sequence (Daselaar et al., 2003).

Section snippets

Methods

All procedures complied with the declaration of Helsinki and medical ethical approval was obtained from the medical ethical committee of the VU University Medical Center. Informed consent was obtained from all subjects.

Effects of selective SWA reduction on sleep parameters

Averaged overall NREM epochs (stages I–IV), the SWA reduction method induced a significant reduction of 4.5 ± 1.5% (mean ± SEM, p = 0.002) in the 0.5–4 Hz SWA band and an increase of (18.6 ± 4.4%, p < 0.001) in the 8–12 Hz alpha band. None of the other bands were affected by the manipulation (see Van Der Werf et al., 2009, for details).

The reduction of SWA was partial and did not lead to a reduction of the duration of stages scored as II, III, or IV, that is, the SWA containing stages. The only significant

Discussion

Disturbances of sleep affect cognitive functioning and psychomotor vigilance. Our results indicate that the effect on performance depends, however, both on the task and on the type of sleep disruption. Selective SWA reduction in individuals without sleep complaints leads to vigilance drops, or lapses, and reduced capacity for encoding novel declarative material while leaving formation of implicit memory intact. The higher number of lapses after SWA reduction parallels the effects of total sleep

Acknowledgments

We thank Dr. Rob Strijers, Mrs. Karin Plugge, and Mrs. Iet Beckmann for their assistance in patient selection.

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