Pathologie Biologie 62 (2014) 241–251

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Insomnia and sleep misperception Insomnie et me´sestimation du sommeil C.H. Bastien a,*,b, T. Ceklic a,b, P. St-Hilaire a,b, F. Desmarais a,c, A.D. Pe´russe a,b, J. Lefranc¸ois a,b, M. Pedneault-Drolet a,b E´cole de psychologie, universite´ Laval, pavillon Fe´lix-Antoine-Savard, bureau 1012, 2325, rue des Bibliothe`ques, G1V 0A6 Que´bec, Canada Laboratoire de neurosciences comportementales humaines, centre de recherche, institut universitaire en sante´ mentale de Que´bec, 2601, chemin de la Canardie`re, G1J 2G3 Que´bec, Que´bec, Canada c ´ Ecole de service social, universite´ Sherbrooke, 2500, boulevard de l’Universite´, J1K 2R1 Sherbrooke, Que´bec, Canada a

b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 7 November 2013 Accepted 9 July 2014 Available online 29 August 2014

Sleep misperception is often observed in insomnia individuals (INS). The extent of misperception varies between different types of INS. The following paper comprised sections which will be aimed at studying the sleep EEG and compares it to subjective reports of sleep in individuals suffering from either psychophysiological insomnia or paradoxical insomnia and good sleeper controls. The EEG can be studied without any intervention (thus using the raw data) via either PSG or fine quantitative EEG analyses (power spectral analysis [PSA]), identifying EEG patterns as in the case of cyclic alternating patterns (CAPs) or by decorticating the EEG while scoring the different transient or phasic events (KComplexes or sleep spindles). One can also act on the on-going EEG by delivering stimuli so to study their impact on cortical measures as in the case of event-related potential studies (ERPs). From the paucity of studies available using these different techniques, a general conclusion can be reached: sleep misperception is not an easy phenomenon to quantify and its clinical value is not well recognized. Still, while none of the techniques or EEG measures defined in the paper is available and/or recommended to diagnose insomnia, ERPs might be the most indicated technique to study hyperarousal and sleep quality in different types of INS. More research shall also be dedicated to EEG patterns and transient phasic events as these EEG scoring techniques can offer a unique insight of sleep misperception. ß 2014 Elsevier Masson SAS. All rights reserved.

Keywords: Sleep Misperception Paradoxical insomnia Psychophysiological insomnia ERP PSA EEG CAP K-Complex Spindle

R E´ S U M E´

Mots cle´s : Sommeil Me´sestimation Insomnie paradoxale Insomnie psychophysiologique ERP PSA EEG CAP Complexe-K Fuseau

La me´sestimation du sommeil est souvent observe´e chez les individus souffrant d’insomnie (INS). Cependant, l’ampleur de cette me´sestimation varie entre les types d’INS. Cet article est compose´ de sections de´die´es a` l’e´tude de l’EEG et sa comparaison avec les rapports subjectifs de sommeil d’individus souffrant soit d’insomnie psychophysiologique ou paradoxale et bons dormeurs. L’EEG peut eˆtre e´tudie´ soit sans intervention (en utilisant les donne´es brutes) comme dans le cas de la polysomnographie ou l’analyse spectrale, soit en identifiant des patrons d’activation comme pour les patrons cycliques alternants (cyclic alternating pattern) ou encore en de´cortiquant l’EEG en e´ve`nements phasiques ou transitoires (complexes-K et fuseaux de sommeil). On peut e´galement agir sur l’EEG en de´livrant des sons et en e´tudiant leur impact sur les ondes de l’EEG comme dans le cas des potentiels e´voque´s, et surtout ceux cognitifs. Du peu d’e´tudes disponibles utilisant ces diffe´rentes techniques/mesures, une conclusion ge´ne´rale peut tout de meˆme eˆtre tire´e : la me´sestimation du sommeil n’est pas facilement quantifiable et sa valeur clinique n’est pas ade´quatement reconnue. Alors qu’aucune des techniques/mesures de´finies ici n’est disponible ou recommande´e afin de diagnostiquer l’insomnie, la technique utilisant les potentiels e´voque´s cognitifs semble la plus approprie´e ou juste afin de mesurer l’hypervigilance corticale

* Corresponding author. E-mail address: [email protected] (C.H. Bastien). http://dx.doi.org/10.1016/j.patbio.2014.07.003 0369-8114/ß 2014 Elsevier Masson SAS. All rights reserved.

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(hyperarousal) et la qualite´ du sommeil chez les diffe´rents types d’individus souffrant d’insomnie. Finalement, plus de recherches devraient eˆtre de´die´es a` l’e´tude des patrons EEG et des e´ve`nements phasiques du sommeil puisque ces techniques apportent une compre´hension diffe´remment unique de la me´sestimation du sommeil. ß 2014 Elsevier Masson SAS. Tous droits re´serve´s.

1. Abbreviations

CAPs DSM-5

Cyclic alternating patterns Diagnostic and Statistical Manual of Mental Disorders – Version 5 Electroencephalogram or electroencephalography EEG Evoked K-Complex EKC Electrooculography EOG Electromyography EMG Event-related potentials ERPs Fast Fourier Transformations FFT functional Magnetic Resonance Imagery (MRI) fMRI Good sleepers GS International Classification of Sleep Disorders ICSD Individuals suffering from insomnia INS K-Complex KC Non-CAP NCAP NREM Non-rapid eye movement Negative wave appearing about 100 milliseconds after N1 stimulus onset Negative wave appearing about 350 milliseconds after N350 stimulus onset PARA-I Paradoxical insomnia sufferers Power spectral analysis PSA Polysomnography PSG Psychophysiological insomnia sufferers PSY-I Positive wave appearing about 200 milliseconds after P2 stimulus onset Positive wave appearing about 300 milliseconds after P3 stimulus onset Rapid eye movement REM Sleep efficiency SE Spontaneous K-Complex SKC Sleep onset-latency SOL SWS Slow wave sleep Stage 2 sleep S2 Total sleep time TST WASO Wake after sleep onset 2. Introduction Insomnia is among the most common health complaints in medical practice. Approximately 30% of the general population experiences some insomnia symptoms occasionally and 10% suffer from chronic and persistent insomnia [1,2]. Frequently reported consequences related to insomnia include fatigue, sleepiness, mood disruption [3], impaired attention and memory deficits [4], consequences being infrequently objectively confirmed [5]. 3. Definition and types of insomnia An insomnia disorder is defined as a complaint of prolonged sleep latency (labeled ‘‘sleep-onset insomnia’’), difficulties in

maintaining sleep (labeled ‘‘sleep-maintenance insomnia’’), waking up too early in the morning (labeled ‘‘terminal insomnia’’), and a mix of different sleep complaints (labeled ‘‘mixed insomnia’’). In addition, the DSM-5 [6] specifies that to be considered a disorder, insomnia or its perceived consequences cause clinically marked distress or significant impairment of occupational or social functioning. Although insomnia can be acute, the current definition of insomnia specifies that it must be present for at least three months. While the International Classification of Sleep Disorders (ICSD) [7] was previously distinguishing among different types of insomnia (Box 1), its new revised version [8] does not recommend a sub-classification of different types for clinical purposes as it mainly argues that empirical evidence is lacking to retain them. As researchers though, it is still strongly believed that at least two types of chronic insomnia (insomnia presenting itself without any other comorbid disorder) warrant attention as they are the most prevalent insomnia types and puzzling [9] and have seemingly different underlying pathophysiology [10–14]. As such, research shall still devote time to their study. These two types are psychophysiological and paradoxical (or sleep-state misperception) insomnia. In some cases, complaints of sleep difficulties are objectively observable, in other cases, they are not. Thus, a patient may either complain of sleep difficulties while objective polysomnographic recordings appear normal, or there may be constant and important gap between objective and subjective measures (for example, polysomnography [PSG] vs sleep diaries) of sleep [9]. As much as 50% of individuals suffering from insomnia could be poor estimators (displaying gross misperception) and classified as paradoxical insomnia sufferers [10,11,15]. While paradoxical INS (PARA-I) and good sleepers (GS) display similar results on measures of sleep macroarchitecture (for example the observed percentage in different sleep stages), there may be subtle differences in their microarchitecture [12]. On the other hand, typically, INS accurately estimating their sleep are those suffering from psychophysiological insomnia (PSY-I). Finally, these two types of INS are not mutually exclusive. Thus, an individual can show objective sleep-onset, sleep-maintenance or mixed objective sleep difficulties once his/her sleep has been recorded in the sleep laboratory but also present important discrepancies between his/ her reports and laboratory sleep observations. As such, an individual might be complaining of mixed sleep difficulties over a long period of time, without showing any signs of depression or anxiety and at the same time, be of the paradoxical type [15]. Unfortunately, it is difficult to estimate the percentage of those

Box 1. Types of insomnia according to the ICSD. Psychophysiological insomnia Paradoxal insomnia Idiopathic insomnia Inadequate sleep hygiene Behavioral insomnia of childhood Insomnia due to (another) mental disorder Insomnia due to (a) medical condition Insomnia due to drug or substance

C.H. Bastien et al. / Pathologie Biologie 62 (2014) 241–251

individuals presenting objective sleep difficulties in addition of gross misperception and, as suggested by St-Jean and Bastien [15], INS sleep difficulties (both objective and subjective) might be better found as distributed along a sleep difficulties ‘continuum’. This paper will introduce and discuss recent experimental research focusing on INS, with a special emphasis on paradoxical insomnia and/or the misperception of sleep. It will first briefly describe PSG results pertaining to INS compared to GS and then provide an overview of the neurophysiological research done in our laboratory and others. This will be achieved by using rigorous criteria so to obtain an homogeneous classification of types of insomnia as is done in our laboratory (see [16]) instead of those suggested by Edinger et al. [9], which are generally non-specific. For example, instead of the liberal sleep-state misperception or paradoxical terms, often only referring to a gross misperception of sleep, PARA-I, in addition of corresponding to the criteria for pure insomnia, will be defined as having:  an objective total sleep time (TST) of more than 6 h 30 min and a sleep efficiency greater than 85% on nocturnal PSG;  showing marked discrepancies between subjective and objective sleep measures (i.e. a difference of 60 min or more for TST, or a difference of at least 15% between subjective and objective measures of sleep efficiency).

The following observation is also common: complaint of severe sleep difficulties most of the time (sleepless nights on sleep diaries being an indicator of severe sleep difficulties). The different criteria presented here for paradoxical insomnia are based on a combination of our research experience (and of what others have also suggested previously – see [10] and [12] for example) and an extension of those suggested by Edinger et al. [9] and Feige et al. [13]. Comparisons with GS, those individuals satisfy with their sleep and not having subjective complaints of sleep difficulties while reporting a sleep efficiency of 85% or more in sleep diaries, and psychophysiological insomnia sufferers (PSY-I), criteria corresponding to those set forward by Edinger et al. [9], are used in our laboratory in order to capture the true essence of sleep misperception. It is our aim to show that important sleep misperception is linked to increased cortical arousal and that PARA-I shall display increased cognitive and electroencephalographic (EEG) arousal compared to PSY-I. The following sections will be aimed at studying the sleep EEG and often comparing it to the subjective reports of sleep of individuals. Also, as is presented below, the EEG can be studied without any intervention (thus just by using the raw data) via either PSG or fine quantitative EEG analyses (power spectral analysis [PSA]), searching for EEG patterns as in the case of cyclic alternating patterns (CAPs) or by decorticating the EEG while scoring the different transient or phasic events such as K-Complex or sleep spindles. On the other hand, one can also act on the ongoing EEG by delivering stimuli so to study the impact on those on cortical measures as in the case of event-related potentials (ERPs) studies. Although these techniques or the study of phasic events in sleep and in insomnia are not usually used in clinical settings or for diagnostic purposes, they still are very helpful in characterizing the pathophysiology of the disorder. Once the pathophysiology of a disorder is well circumscribed or at least, better understood, it is then easier to design effective treatments or even prevent the appearance of the disorder. Thus clinical considerations will not be explored here, only research ones. However, before detailing every technique, the basis and the definition of insomnia in research is presented with the subjective ratings of sleep. We will then introduce each technique which will begin with a brief definition and then move to the different studies related to sleep and to its

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misperception in insomnia, when available. Finally, each section reaches a conclusion on presented results. 4. Sleep diary A detailed clinical history/assessment of the patient’s subjective complaint will significantly benefit complementary data from more systematic sources such neurophysiological and neuropsychological assessments. Sleep diary monitoring is an exceptional tool to document the perceived severity of insomnia. A sleep diary commonly requires self-recording of bedtime and arising time, along with morning estimates of sleep-onset latency, number and duration of awakenings, total sleep time, and several indices of sleep quality for the previous night. Even though they do not reflect absolute values obtained from polysomnography (see Appendix A), daily morning estimates of sleep parameters such as sleep-onset latency or wake after sleep-onset yield a reliable and valid index of insomnia [17]. A sleep diary also captures the night-to-night variability that often characterizes the sleep of chronic INS [18–20] compared to one or two nights of polysomnography. Of course, for paradoxical insomnia individuals, sleep diaries are often characterized by sleep disturbances on each and every night and good nights are very rare. In addition, we have previously shown that sleepless nights are often reported by PARA-I [21]. A sleep efficiency (total sleep time divided by time in bed) lower than 85% also characterizes INS. Based on the diary measures, sleeponset (SOL) insomnia was typically defined by a latency to sleeponset of at least 30 minutes, and sleep-maintenance insomnia was defined by time awake after sleep-onset (WASO) of at least 30 minutes. With the introduction of the DSM-5 and the ISCD-III, the reported sleep disturbance, either for SOL or for WASO, can be as low as of 20 minutes. On the other hand, early morning awakening can be operationalized by a complaint of waking up earlier than desired, with an inability to go back to sleep, and before total sleep time reaches 6.5 h. These criteria, while seemingly arbitrary, are useful to operationalize the definition of insomnia. 5. Polysomnography (PSG) Insomnia protocols are usually conducted on two or three consecutive nights of PSG recordings. Usual PSG recordings include electroencephalography (EEG), electrooculography (EOG) and electromyography (EMG). PSG has two main objectives:  codify the different NREM sleep (stages 1, 2, 3 and 4) and REM sleep (Fig. 1);  screen for sleep disorders and quantify their respective severities. One important limitation of PSG is that it does not provide a valid sample of an individual’s typical sleep, and especially for INS. Actually, the sleep of GS is more disrupted during their first night of recording in the sleep laboratory (i.e., first night effect: worst sleep efficiency on the first night compared to subsequent ones), while the sleep of INS may actually improve (i.e., reverse first night effect: better sleep efficiency on the first night than on subsequent ones) [22]. Still, PSG is particularly helpful for studying types of insomnia, for example when studying PARA-I, since, by definition, it entails large discrepancies between objective and subjective estimates of sleep. Our own research group has suggested that paradoxical insomnia is best identified after large subjectiveobjective discrepancies have been observed on at least two out of four consecutive recording nights in the laboratory [16]. In any case, modest PSG differences are generally observed between INS and GS, INS tending to spend more time in stage 1, less time in

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Fig. 1. Signals (channels) recorded from the participant displayed in this figures are those often used for scoring of sleep stages. Fp1 and Fp2 correspond respectively to left and right eye of electromyographic recordings (EOG). Subsequent channels include EEG leads (C3, C4, O1 and O2), EMG activity from the right chin (EMGr), left and right tibialis for leg movements (Lleg and Rleg), thoracic and abdominal bands for respiratory efforts. Tibialis and respiratory efforts are used to respectively obtain indexes for PLMS and apneoa/hypopnoea. The sleeping individual is presently in stage 4 sleep (eye movements following the EEG, high amplitude EEG – SWS and delta – and decreased EMG). In the white box, at the top of the figure, the all night hypnogram is displayed.

stages 3–4, and show more frequent stage shifts through the night [17,23,24]. During the day, our group has recently provided empirical evidence that both PSY-I and PARA-I differ on PSG measures from GS during napping [25]. These results are encouraging and do suggest that insomnia is a 24-hour problem and dividing INS in types might be quite informative about cortical processes at play. Nonetheless, because of limited between group differences observed so far between INS and GS on objective measures of sleep, it is very much suggested to use finer EEG or quantitative techniques to uncover cortical differences between INS and GS and also between PSY-I and PARA-I. Even if PSG has been considered the gold standard for a long time, it is usually unavailable on a day-to-day basis and for clinical diagnosis. In addition, because of contradictory results between labs for INS (all types combined) and GS in PSG recordings, PSG is recommended only in insomnia research and not in clinical settings, unless, of course, another sleep disorders is suspected. In addition, since information provided through PSG is limited, other finer cortical measures are needed to disentangle between subjective and objective insomnia and ‘quantify’ sleep misperception. One of these techniques is the study of cognitive information processing with event-related potentials (ERPs; Fig. 2).

and attention, and later components usually reflect higher order central nervous system processing related to cognitive functions [26]. The valence and latency of peaks are used to label the different components: ‘‘N’’ refers to a negative wave and ‘‘P’’ to a positive wave. Thus, for example, ‘‘N100’’ would refer to a negative wave appearing 100 ms after stimulus onset (note that ERPs are usually termed as N1, P2, P3 even though their respective latency is 100, 200 and 300 ms). A cognitive process (or role) is associated with most ERP, common processes being attention (N1), inhibition

6. Event-related potentials (ERPs) An external physical stimulus or internal psychological event elicits small amplitude changes in the EEG, therefore providing a means to ‘‘probe’’ the extent of information processing within the nervous system during wake and sleep. Contrary to neuroimaging, which has an excellent spatial resolution, event-related potentials (ERPs) have a high temporal resolution (about one tenth of a millisecond). ERP components are classified according to their latencies: early components (

Insomnia and sleep misperception.

Sleep misperception is often observed in insomnia individuals (INS). The extent of misperception varies between different types of INS. The following ...
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