ABSTRACT
By connecting old and recent notions, different spatial scales, and research domains, we introduce a novel framework on the consequences of brain injury focusing on a key role of slow waves. We argue that the long-standing finding of EEG slow waves after brain injury reflects the intrusion of sleep-like cortical dynamics during wakefulness; we illustrate how these dynamics are generated and how they can lead to functional network disruption and behavioral impairment. Finally, we outline a scenario whereby post-injury slow waves can be modulated to reawaken parts of the brain that have fallen asleep to optimize rehabilitation strategies and promote recovery.
Subject(s)
Brain Injuries , Electroencephalography , Sleep , Wakefulness , Wakefulness/physiology , Humans , Brain Injuries/physiopathology , Sleep/physiology , Cerebral Cortex/physiopathology , Animals , Brain/physiopathology , Nerve Net/physiopathologyABSTRACT
STUDY OBJECTIVES: To collect prodromal symptoms experienced by participants with narcolepsy and idiopathic hypersomnia (considered "hypersomnolence experts") prior to drowsy driving and counter-strategies used to maintain alertness. METHODS: Systematic, face-to-face interview (using a semi-structured questionnaire), including clinical measures, frequency of car accidents/near misses, and symptoms experienced before impending drowsy driving episodes and counter-strategies. RESULTS: Among 61 participants (32 with narcolepsy, 29 with idiopathic hypersomnia; 56 drivers), 61% of drivers had at least one lifetime accident/near miss. They had a higher sleepiness score (14 ± 4 vs. 11 ± 5, P<0.04) than those without an accident/near miss, but no other differences in demographics, driving experience, medical conditions, symptoms, sleep tests, and treatment. All but three participants experienced prodromal symptoms of drowsy driving, which included postural and motor changes (86.9%: axial hypotonia - e.g., eyelid droop, stereotyped movements), cognitive impairment (53.3%: automatic steering, difficulty concentrating/shifting, dissociation, mind wandering, dreaming), sensory (65%: paresthesia, pain, stiffness, heaviness, blunted perceptions such as a flat dashboard with loss of 3D, illusions and hallucinations), and autonomic symptoms (10%, altered heart/breath rate, penile erection). Counterstrategies included self-stimulation from external sources (pain, cold air, music, drinks, driving with bare feet), motor changes (upright posture, movements), and surprise (sudden braking). CONCLUSIONS: Drowsy driving symptoms can result from "local" NREM, entry in N1 sleep, and hybrid wake/REM sleep states. These rich qualitative insights from participants with narcolepsy and idiopathic hypersomnia, as well as sophisticated counter-strategies, can be gathered to reduce the crash risk in this population, but also in inexperienced healthy drivers.
ABSTRACT
The transition from wakefulness to sleep is a progressive process that is reflected in the gradual loss of responsiveness, an alteration of cognitive functions, and a drastic shift in brain dynamics. These changes do not occur all at once. The sleep onset period (SOP) refers here to this period of transition between wakefulness and sleep. For example, although transitions of brain activity at sleep onset can occur within seconds in a given brain region, these changes occur at different time points across the brain, resulting in a SOP that can last several minutes. Likewise, the transition to sleep impacts cognitive and behavioral levels in a graded and staged fashion. It is often accompanied and preceded by a sensation of drowsiness and the subjective feeling of a need for sleep, also associated with specific physiological and behavioral signatures. To better characterize fluctuations in vigilance and the SOP, a multidimensional approach is thus warranted. Such a multidimensional approach could mitigate important limitations in the current classification of sleep, leading ultimately to better diagnoses and treatments of individuals with sleep and/or vigilance disorders. These insights could also be translated in real-life settings to either facilitate sleep onset in individuals with sleep difficulties or, on the contrary, prevent or control inappropriate sleep onsets.
Subject(s)
Sleepiness , Wakefulness , Humans , Wakefulness/physiology , Sleep/physiology , Brain/physiology , CognitionABSTRACT
Sleep deprivation has an ever-increasing impact on individuals and societies. Yet, to date, there is no quick and objective test for sleep deprivation. Here, we used automated acoustic analyses of the voice to detect sleep deprivation. Building on current machine-learning approaches, we focused on interpretability by introducing two novel ideas: the use of a fully generic auditory representation as input feature space, combined with an interpretation technique based on reverse correlation. The auditory representation consisted of a spectro-temporal modulation analysis derived from neurophysiology. The interpretation method aimed to reveal the regions of the auditory representation that supported the classifiers' decisions. Results showed that generic auditory features could be used to detect sleep deprivation successfully, with an accuracy comparable to state-of-the-art speech features. Furthermore, the interpretation revealed two distinct effects of sleep deprivation on the voice: changes in slow temporal modulations related to prosody and changes in spectral features related to voice quality. Importantly, the relative balance of the two effects varied widely across individuals, even though the amount of sleep deprivation was controlled, thus confirming the need to characterize sleep deprivation at the individual level. Moreover, while the prosody factor correlated with subjective sleepiness reports, the voice quality factor did not, consistent with the presence of both explicit and implicit consequences of sleep deprivation. Overall, the findings show that individual effects of sleep deprivation may be observed in vocal biomarkers. Future investigations correlating such markers with objective physiological measures of sleep deprivation could enable "sleep stethoscopes" for the cost-effective diagnosis of the individual effects of sleep deprivation.
Subject(s)
Sleep Deprivation , Voice , Humans , Sleep , Voice Quality , WakefulnessABSTRACT
The ability to detect and subsequently correct errors is important in preventing the detrimental consequences of sleep loss. The Error Related Negativity (ERN), and the error positivity (Pe) are established neural correlates of error processing. Previous work has shown sleep loss reduces ERN and Pe, indicating sleep loss impairs error-monitoring processes. However, no previous work has examined behavioral error awareness, in conjunction with EEG measures, under sleep loss conditions, and studies of sleep restriction are lacking. Using combined behavioral and EEG measures, we report two studies investigating the impact of total sleep deprivation (TSD) and sleep restriction (SR) on error awareness. Fourteen healthy participants completed the Error Awareness Task under conditions of TSD and 27 completed the same task under conditions of SR. It was found that TSD did not influence behavioral error awareness or ERN or Pe amplitude, however, SR reduced behavioral error awareness, increased the time taken to detect errors, and reduced Pe amplitude. Findings indicate individuals who are chronically sleep restricted are at risk for reduced recognition of errors. Reduced error awareness may be one factor contributing to the increased accidents and injuries seen in contexts where sleep loss is prevalent.
Subject(s)
Electroencephalography , Evoked Potentials , Humans , Reaction Time , Sleep Deprivation , Sleep , Psychomotor Performance , AwarenessABSTRACT
Wakefulness, non-rapid eye-movement (NREM) and rapid eye-movement (REM) sleep differ from each other along three dimensions: behavioral, phenomenological, physiological. Although these dimensions often fluctuate in step, they can also dissociate. The current paradigm that views sleep as made of global NREM and REM states fail to account for these dissociations. This conundrum can be dissolved by stressing the existence and significance of the local regulation of sleep. We will review the evidence in animals and humans, healthy and pathological brains, showing different forms of local sleep and the consequences on behavior, cognition, and subjective experience. Altogether, we argue that the notion of local sleep provides a unified account for a host of phenomena: dreaming in REM and NREM sleep, NREM and REM parasomnias, intrasleep responsiveness, inattention and mind wandering in wakefulness. Yet, the physiological origins of local sleep or its putative functions remain unclear. Exploring further local sleep could provide a unique and novel perspective on how and why we sleep.
Subject(s)
Sleep, REM , Sleep , Animals , Humans , Sleep, REM/physiology , Brain , Wakefulness/physiology , Cognition/physiology , ElectroencephalographyABSTRACT
STUDY OBJECTIVES: Insomnia is a disorder diagnosed based on self-reported sleep complaints. Differences between self-reported and sensor-based sleep parameters (sleep-wake state discrepancy) are common but not well-understood in individuals with insomnia. This two-arm, parallel-group, single-blind, superiority randomized-controlled trial examined whether monitoring sleep using wearable devices and providing support for interpretation of sensor-based sleep data improved insomnia symptoms or impacted sleep-wake state discrepancy. METHODS: A total of 113 (age M = 47.53; SD = 14.37, 64.9% female) individuals with significant insomnia symptoms (Insomnia Severity Index(ISI) ≥10) from the community were randomized 1:1 (permuted block randomization) to receive 5 weeks (1) Intervention (n = 57): feedback about sensor-based sleep (Fitbit and EEG headband) with guidance for data interpretation and ongoing monitoring, and (2) Control (n = 56): sleep education and hygiene. Both groups received one individual session and two check-in calls. The ISI (primary outcome), sleep disturbance (SDis), sleep-related impairment (SRI), depression, and anxiety were assessed at baseline and post-intervention. RESULTS: In total, 103 (91.2%) participants completed the study. Intention-to-treat multiple regression with multiple imputations showed that after controlling for baseline values, compared to the Control group (n = 51), the Intervention group (n = 52) had lower ISI (p = .011, d = 0.51) and SDis (p = .036, d = 0.42) post-intervention, but differences in SRI, depression, anxiety, and sleep-wake state discrepancy parameters (total sleep time, sleep onset latency, and wake after sleep onset) were not meaningful (P-values >.40). CONCLUSIONS: Providing feedback and guidance about sensor-based sleep parameters reduced insomnia severity and sleep disturbance but did not alter sleep-wake state discrepancy in individuals with insomnia more than sleep hygiene and education. The role of sleep wearable devices among individuals with insomnia requires further research. CLINICAL TRIAL REGISTRATION: The Novel Insomnia Treatment Experiment (NITE): the effectiveness of incorporating appropriate guidance for sleep wearables in users with insomnia. https://www.anzctr.org.au/Trial/Registration/TrialReview.aspx?id=378452, Australia New Zealand Clinical Trials Registry: ACTRN12619001636145.
Subject(s)
Sleep Initiation and Maintenance Disorders , Humans , Female , Male , Sleep Initiation and Maintenance Disorders/complications , Sleep Initiation and Maintenance Disorders/therapy , Feedback , Single-Blind Method , Sleep , Polysomnography , Treatment OutcomeABSTRACT
Study Objectives: Insomnia is common in the general population and is diagnosed based on self-reported sleep complaints. There is a frequent discrepancy between objectively recorded and self-reported sleep (sleep-wake state discrepancy), especially in individuals with insomnia. Although sleep-wake state discrepancy is well-documented in the literature, it is not well understood. This protocol describes the methodology of a randomized control study, which will examine whether providing monitoring and feedback about objectively recorded sleep with support for interpretation of sleep-wake state discrepancy improves insomnia symptoms and will explore the potential mechanisms of change. Methods: Participants are 90 individuals with insomnia symptoms (Insomnia Severity Index [ISI] ≥10). Participants will be randomized to one of two conditions: (1) Intervention: feedback about objectively recorded sleep (actigraph and optional electroencephalogram headband) with guidance for data interpretation, (2) Control: sleep hygiene session. Both conditions will involve individual sessions and two check-in calls. The primary outcome is ISI score. Secondary outcomes include sleep-related impairment, symptoms of anxiety and depression, and other sleep and quality of life measures. Outcomes will be assessed using validated instruments at baseline and post-intervention. Discussion: With increasing number of wearable devices that measure sleep, there is a need to understand how sleep data provided by these devices could be utilized in the treatment of insomnia. Findings from this study have the potential to better understand sleep-wake state discrepancy in insomnia and uncover new approaches to supplement current insomnia treatment.
ABSTRACT
Online speech processing imposes significant computational demands on the listening brain, the underlying mechanisms of which remain poorly understood. Here, we exploit the perceptual "pop-out" phenomenon (i.e. the dramatic improvement of speech intelligibility after receiving information about speech content) to investigate the neurophysiological effects of prior expectations on degraded speech comprehension. We recorded electroencephalography (EEG) and pupillometry from 21 adults while they rated the clarity of noise-vocoded and sine-wave synthesized sentences. Pop-out was reliably elicited following visual presentation of the corresponding written sentence, but not following incongruent or neutral text. Pop-out was associated with improved reconstruction of the acoustic stimulus envelope from low-frequency EEG activity, implying that improvements in perceptual clarity were mediated via top-down signals that enhanced the quality of cortical speech representations. Spectral analysis further revealed that pop-out was accompanied by a reduction in theta-band power, consistent with predictive coding accounts of acoustic filling-in and incremental sentence processing. Moreover, delta-band power, alpha-band power, and pupil diameter were all increased following the provision of any written sentence information, irrespective of content. Together, these findings reveal distinctive profiles of neurophysiological activity that differentiate the content-specific processes associated with degraded speech comprehension from the context-specific processes invoked under adverse listening conditions.
Subject(s)
Motivation , Speech Perception , Noise , Electroencephalography , Acoustic Stimulation , Speech Intelligibility/physiology , Speech Perception/physiologyABSTRACT
Every night, we pass through a transitory zone at the borderland between wakefulness and sleep, named the first stage of nonrapid eye movement sleep (N1). N1 sleep is associated with increased hippocampal activity and dream-like experiences that incorporate recent wake materials, suggesting that it may be associated with memory processing. Here, we investigated the specific contribution of N1 sleep in the processing of memory traces. Participants were asked to learn the precise locations of 48 objects on a grid and were then tested on their memory for these items before and after a 30-min rest during which participants either stayed fully awake or transitioned toward N1 or deeper (N2) sleep. We showed that memory recall was lower (10% forgetting) after a resting period, including only N1 sleep compared to N2 sleep. Furthermore, the ratio of alpha/theta power (an electroencephalography marker of the transition toward sleep) correlated negatively with the forgetting rate when taking into account all sleepers (N1 and N2 groups combined), suggesting a physiological index for memory loss that transcends sleep stages. Our findings suggest that interrupting sleep onset at N1 may alter sleep-dependent memory consolidation and promote forgetting.
ABSTRACT
Sustained attention describes our ability to keep a constant focus on a given task. This ability is modulated by our physiological state of arousal. Although lapses of sustained attention have been linked with dysregulations of arousal, the underlying physiological mechanisms remain unclear. An emerging body of work proposes that the intrusion during wakefulness of sleep-like slow waves, a marker of the transition toward sleep, could mechanistically account for attentional lapses. This study aimed to expose, via pharmacological manipulations of the monoamine system, the relationship between the occurrence of sleep-like slow waves and the behavioral consequences of sustained attention failures. In a double-blind, randomized-control trial, 32 healthy human male participants received methylphenidate, atomoxetine, citalopram or placebo during four separate experimental sessions. During each session, electroencephalography (EEG) was used to measure neural activity while participants completed a visual task requiring sustained attention. Methylphenidate, which increases wake-promoting dopamine and noradrenaline across cortical and subcortical areas, improved behavioral performance whereas atomoxetine, which increases dopamine and noradrenaline predominantly over frontal cortices, led to more impulsive responses. Additionally, citalopram, which increases sleep-promoting serotonin, led to more missed trials. Based on EEG recording, citalopram was also associated with an increase in sleep-like slow waves. Importantly, compared with a classical marker of arousal such as α power, only slow waves differentially predicted both misses and faster responses in a region-specific fashion. These results suggest that a decrease in arousal can lead to local sleep intrusions during wakefulness which could be mechanistically linked to impulsivity and sluggishness.SIGNIFICANCE STATEMENT We investigated whether the modulation of attention and arousal could not only share the same neuromodulatory pathways but also rely on similar neuronal mechanisms; for example, the intrusion of sleep-like activity within wakefulness. To do so, we pharmacologically manipulated noradrenaline, dopamine, and serotonin in a four-arm, randomized, placebo-controlled trial and examined the consequences on behavioral and electroencephalography (EEG) indices of attention and arousal. We showed that sleep-like slow waves can predict opposite behavioral signatures: impulsivity and sluggishness. Slow waves may be a candidate mechanism for the occurrence of attentional lapses since the relationship between slow-wave occurrence and performance is region-specific and the consequences of these local sleep intrusions are in line with the cognitive functions carried by the underlying brain regions.
Subject(s)
Citalopram , Methylphenidate , Male , Humans , Citalopram/pharmacology , Dopamine , Atomoxetine Hydrochloride/pharmacology , Serotonin , Sleep/physiology , Wakefulness/physiology , Electroencephalography/methods , Attention , Norepinephrine , Methylphenidate/pharmacologyABSTRACT
The widely used guidelines for sleep staging were developed for the visual inspection of electrophysiological recordings by the human eye. As such, these rules reflect a limited range of features in these data and are therefore restricted in accurately capturing the physiological changes associated with sleep. Here we present a novel analysis framework that extensively characterizes sleep dynamics using over 7700 time-series features from the hctsa software. We used clustering to categorize sleep epochs based on the similarity of their time-series features, without relying on established scoring conventions. The resulting sleep structure overlapped substantially with that defined by visual scoring. However, we also observed discrepancies between our approach and traditional scoring. This divergence principally stemmed from the extensive characterization by hctsa features, which captured distinctive time-series properties within the traditionally defined sleep stages that are overlooked with visual scoring. Lastly, we report time-series features that are highly discriminative of stages. Our framework lays the groundwork for a data-driven exploration of sleep sub-stages and has significant potential to identify new signatures of sleep disorders and conscious sleep states.
Subject(s)
Electroencephalography , Sleep Stages , Cluster Analysis , Electroencephalography/methods , Humans , Polysomnography/methods , Sleep/physiology , Sleep Stages/physiology , Time FactorsABSTRACT
The pupillary light response is an important automatic physiological response which optimizes light reaching the retina. Recent work has shown that the pupil also adjusts in response to illusory brightness and a range of cognitive functions, however, it remains unclear what exactly drives these endogenous changes. Here, we show that the imagery pupillary light response correlates with objective measures of sensory imagery strength. Further, the trial-by-trial phenomenological vividness of visual imagery is tracked by the imagery pupillary light response. We also demonstrated that a group of individuals without visual imagery (aphantasia) do not show any significant evidence of an imagery pupillary light response, however they do show perceptual pupil light responses and pupil dilation with larger cognitive load. Our results provide evidence that the pupillary light response indexes the sensory strength of visual imagery. This work also provides the first physiological validation of aphantasia.
Subject(s)
Imagination , Pupil , Cognition/physiology , Humans , Imagery, Psychotherapy , Imagination/physiology , Visual Perception/physiologyABSTRACT
The ability to think creatively is paramount to facing new challenges, but how creativity arises remains mysterious. Here, we show that the brain activity common to the twilight zone between sleep and wakefulness (nonrapid eye movement sleep stage 1 or N1) ignites creative sparks. Participants (N = 103) were exposed to mathematical problems without knowing that a hidden rule allowed solving them almost instantly. We found that spending at least 15 s in N1 during a resting period tripled the chance to discover the hidden rule (83% versus 30% when participants remained awake), and this effect vanished if subjects reached deeper sleep. Our findings suggest that there is a creative sweet spot within the sleep-onset period, and hitting it requires individuals balancing falling asleep easily against falling asleep too deeply.
ABSTRACT
What makes a good night's sleep? It is often assumed that sleep is the deepest when brain activity is dominated by hyper-synchronized slow waves. However, sleep appears subjectively the deepest in rapid eye movement (REM) sleep, when slow waves are absent.
Subject(s)
Sleep , Wakefulness , Emotions , Sleep, REMABSTRACT
BACKGROUND: Many scientific fields now use machine-learning tools to assist with complex classification tasks. In neuroscience, automatic classifiers may be useful to diagnose medical images, monitor electrophysiological signals, or decode perceptual and cognitive states from neural signals. However, such tools often remain black-boxes: they lack interpretability. A lack of interpretability has obvious ethical implications for clinical applications, but it also limits the usefulness of these tools to formulate new theoretical hypotheses. NEW METHOD: We propose a simple and versatile method to help characterize the information used by a classifier to perform its task. Specifically, noisy versions of training samples or, when the training set is unavailable, custom-generated noisy samples, are fed to the classifier. Multiplicative noise, so-called "bubbles", or additive noise are applied to the input representation. Reverse correlation techniques are then adapted to extract either the discriminative information, defined as the parts of the input dataset that have the most weight in the classification decision, and represented information, which correspond to the input features most representative of each category. RESULTS: The method is illustrated for the classification of written numbers by a convolutional deep neural network; for the classification of speech versus music by a support vector machine; and for the classification of sleep stages from neurophysiological recordings by a random forest classifier. In all cases, the features extracted are readily interpretable. COMPARISON WITH EXISTING METHODS: Quantitative comparisons show that the present method can match state-of-the art interpretation methods for convolutional neural networks. Moreover, our method uses an intuitive and well-established framework in neuroscience, reverse correlation. It is also generic: it can be applied to any kind of classifier and any kind of input data. CONCLUSIONS: We suggest that the method could provide an intuitive and versatile interface between neuroscientists and machine-learning tools.
Subject(s)
Machine Learning , Neural Networks, Computer , Support Vector MachineABSTRACT
Attentional lapses occur commonly and are associated with mind wandering, where focus is turned to thoughts unrelated to ongoing tasks and environmental demands, or mind blanking, where the stream of consciousness itself comes to a halt. To understand the neural mechanisms underlying attentional lapses, we studied the behaviour, subjective experience and neural activity of healthy participants performing a task. Random interruptions prompted participants to indicate their mental states as task-focused, mind-wandering or mind-blanking. Using high-density electroencephalography, we report here that spatially and temporally localized slow waves, a pattern of neural activity characteristic of the transition toward sleep, accompany behavioural markers of lapses and preceded reports of mind wandering and mind blanking. The location of slow waves could distinguish between sluggish and impulsive behaviours, and between mind wandering and mind blanking. Our results suggest attentional lapses share a common physiological origin: the emergence of local sleep-like activity within the awake brain.
Subject(s)
Attention/physiology , Sleep, Slow-Wave/physiology , Adult , Behavior/physiology , Brain/physiology , Electroencephalography , Female , Humans , Male , Models, Psychological , Task Performance and Analysis , Wakefulness/physiologyABSTRACT
Awareness of performance deficits and errors during sleep loss could be protective against the consequences of sleep deprivation, however, it is unclear whether sleep deprived individuals have insight into their performance. We conducted a systematic review and meta-analysis of the impact of sleep loss (sleep duration <6 h) on monitoring of performance and errors using Embase, MEDLINE, PsycINFO & Cochrane Central. We identified 28 studies, 11 of which were appropriate for meta-analysis. The systematic review indicated limited consensus regarding sleep loss impacts on performance monitoring, due to substantial differences in study methodology. However, participants typically demonstrated more conservative estimates of performance during sleep loss. Error-monitoring literature was more consistent, indicating an impairment in error-monitoring following sleep loss. Meta-analyses supported the findings of the systematic review. In terms of methodology, we found the performance monitoring literature is limited by an overreliance on correlational designs, which are likely confounded by response bias. The error-monitoring literature is limited by very few studies utilising behavioural measures to directly measure error-awareness. Future performance monitoring studies must employ methods which control for confounds such as bias, and error-monitoring studies must incorporate combined behavioural and ERP measures to better understand the impact of sleep loss on error-monitoring.
Subject(s)
Sleep Initiation and Maintenance Disorders , Humans , Sleep , Sleep DeprivationABSTRACT
For most people, visual imagery is an innate feature of many of our internal experiences, and appears to play a critical role in supporting core cognitive processes. Some individuals, however, lack the ability to voluntarily generate visual imagery altogether - a condition termed "aphantasia". Recent research suggests that aphantasia is a condition defined by the absence of visual imagery, rather than a lack of metacognitive awareness of internal visual imagery. Here we further illustrate a cognitive "fingerprint" of aphantasia, demonstrating that compared to control participants with imagery ability, aphantasic individuals report decreased imagery in other sensory domains, although not all report a complete lack of multi-sensory imagery. They also report less vivid and phenomenologically rich autobiographical memories and imagined future scenarios, suggesting a constructive role for visual imagery in representing episodic events. Interestingly, aphantasic individuals report fewer and qualitatively impoverished dreams compared to controls. However, spatial abilities appear unaffected, and aphantasic individuals do not appear to be considerably protected against all forms of trauma symptomatology in response to stressful life events. Collectively, these data suggest that imagery may be a normative representational tool for wider cognitive processes, highlighting the large inter-individual variability that characterises our internal mental representations.