Temporary amnesia from sleep loss: A framework for understanding consequences of sleep deprivation.

Throughout its modern history, sleep research has been concerned with both the benefits of sleep and the deleterious impact of sleep disruption for cognition, behavior, and performance. When more specifically examining the impact of sleep on memory and learning, however, research has overwhelmingly focused on how sleep following learning facilitates memory, with less attention paid to how lack of sleep prior to learning can disrupt subsequent memory. Although this imbalance in research emphasis is being more frequently addressed by current investigators, there is a need for a more organized approach to examining the effect of sleep deprivation before learning. The present review briefly describes the generally accepted approach to analyzing effects of sleep deprivation on subsequent memory and learning by means of its effects on encoding. Then, we suggest an alternative framework with which to understand sleep loss and memory in terms of temporary amnesia from sleep loss (TASL). The review covers the well-characterized properties of amnesia arising from medial temporal lobe lesions and shows how the pattern of preserved and impaired aspects of memory in amnesia may also be appearing during sleep loss. The view of the TASL framework is that amnesia and the amnesia-like deficits observed during sleep deprivation not only affect memory processes but will also be apparent in cognitive processes that rely on those memory processes, such as decision-making. Adoption of the TASL framework encourages movement away from traditional explanations based on narrowly defined domains of memory functioning, such as encoding, and taking instead a more expansive view of how brain structures that support memory, such as the hippocampus, interact with higher structures, such as the prefrontal cortex, to produce complex cognition and behavioral performance, and how this interaction may be compromised by sleep disruption.

Effects of total sleep deprivation on components of top-down attentional control using a flexible attentional control task.

Sleep deprivation consistently decreases vigilant attention, which can lead to difficulty in performing a variety of cognitive tasks. However, sleep-deprived individuals may be able to compensate for degraded vigilant attention by means of top-down attentional control. We employed a novel task to measure the degree to which individuals overcome impairments in vigilant attention by using top-down attentional control, the Flexible Attentional Control Task (FACT). The FACT is a two-choice task that has trials with valid, invalid, and neutral cues, along with an unexpected switch in the probability of cue validity about halfway in the task. The task provides indices that isolate performance components reflecting vigilant attention and top-down attentional control. Twelve healthy young adults completed an in-laboratory study. After a baseline day, the subjects underwent 39 hours of total sleep deprivation (TSD), followed by a recovery day. The FACT was administered at 03:00, 11:00, and 19:00 during sleep deprivation (TSD condition) and at 11:00 and 19:00 after baseline sleep and at 11:00 after recovery sleep (rested condition). When rested, the subjects demonstrated both facilitation and interference effects on cued trials. While sleep deprived, the subjects showed vigilant attention deficits on neutral cue trials, and an impaired ability to reduce these deficits by using predictive contextual cues. Our results indicate that the FACT can dissociate vigilant attention from top-down attentional control. Furthermore, they show that during sleep deprivation, contextual cues help individuals to compensate partially for impairments in vigilant attention, but the effectiveness of top-down attentional control is diminished.

Electrodermal Activity Is Sensitive to Sleep Deprivation but Does Not Moderate the Effect of Total Sleep Deprivation on Affect.

Emotion is characterized by dimensions of affective valence and arousal, either or both of which may be altered by sleep loss, thereby contributing to impaired regulatory functioning. Controlled laboratory studies of total sleep deprivation (TSD) generally show alterations in physiological arousal and affective state, but the relationship of affect and emotion with physiological arousal during TSD has not been well characterized. Established methods for examining physiological arousal include electrodermal activity (EDA) measures such as non-specific skin conductance responses (NSSCR) and skin conductance level (SCL). These measures are robust physiological markers of sympathetic arousal and have been linked to changes in experienced emotion. To explore the link between physiological arousal and affect during sleep deprivation, we investigated individuals' EDA under TSD and its relationship to self-reported affect. We also investigated the relationship of EDA to two other measures known to be particularly sensitive to the arousal-decreasing effects of TSD, i.e., self-reported sleepiness and performance on a vigilant attention task. Data were drawn from three previously published laboratory experiments where participants were randomly assigned to either well-rested control (WRC) or 38 h of TSD. In this data set, comprising one of the largest samples ever used in an investigation of TSD and EDA (N = 193 with 74 WRC and 119 TSD), we found the expected impairing effects of TSD on self-reported affect and sleepiness and on vigilant attention. Furthermore, we found that NSSCR, but not SCL, were sensitive to TSD, with significant systematic inter-individual differences. Across individuals, the change in frequency of NSSCR during TSD was not predictive of the effect of TSD on affect, sleepiness, or vigilant attention, nor was it related to these outcomes during the rested baseline. Our findings indicate that while physiological arousal, as measured by EDA, may be useful for assessing TSD-related changes in non-specific arousal at the group level, it is not associated with individuals' self-reported affect at rest nor their change in affect during TSD. This suggests that an essential aspect of the relationship between physiological arousal and self-reported affect is not well captured by EDA as measured by NSSCR.

Total sleep deprivation reduces top-down regulation of emotion without altering bottom-up affective processing.

Sleep loss is reported to influence affective processing, causing changes in overall mood and altering emotion regulation. These aspects of affective processing are seldom investigated together, making it difficult to determine whether total sleep deprivation has a global effect on how affective stimuli and emotions are processed, or whether specific components of affective processing are affected selectively. Sixty healthy adults were recruited for an in-laboratory study and, after a monitored night of sleep and laboratory acclimation, randomly assigned to either a total sleep deprivation condition (n = 40) or a rested control condition (n = 20). Measurements of mood, vigilant attention to affective stimuli, affective working memory, affective categorization, and emotion regulation were taken for both groups. With one exception, measures of interest were administered twice: once at baseline and again 24 hours later, after the sleep deprived group had spent a night awake (working memory was assessed only after total sleep deprivation). Sleep deprived individuals experienced an overall reduction in positive affect with no significant change in negative affect. Despite the substantial decline in positive affect, there was no evidence that processing affectively valenced information was biased under total sleep deprivation. Sleep deprived subjects did not rate affective stimuli differently from rested subjects, nor did they show sleep deprivation-specific effects of affect type on vigilant attention, working memory, and categorization tasks. However, sleep deprived subjects showed less effective regulation of negative emotion. Overall, we found no evidence that total sleep deprivation biased the processing of affective stimuli in general. By contrast, total sleep deprivation appeared to reduce controlled processing required for emotion regulation.

Sleep deprivation impairs binding of information with its context.

Binding information to its context in long-term memory is critical for many tasks, including memory tasks and decision making. Failure to associate information to its context could be an important aspect of sleep deprivation effects on cognition, but little is known about binding problems from being sleep-deprived at the time of encoding. We studied how sleep deprivation affects binding using a well-established paradigm testing the ability to remember auditorily presented words (items) and their speakers (source context). In a laboratory study, 68 healthy young adults were randomly assigned to total sleep deprivation or a well-rested control condition. Participants completed an affective item and source memory task twice: once after 7-hour awake during baseline and again 24 hours later, after nearly 31 hours awake in the total sleep deprivation condition or 7 hours awake in the control condition. Participants listened to negative, positive, and neutral words presented by a male or female speaker and were immediately tested for recognition of the words and their respective speakers. Recognition of items declined during sleep deprivation, but even when items were recognized accurately, recognition of their associated sources also declined. Negative items were less bound with their sources than positive or neutral items, but sleep deprivation did not significantly affect this pattern. Our findings indicate that learning while sleep-deprived disrupts the binding of information to its context independent of item valence. Such binding failures may contribute to sleep deprivation effects on tasks requiring the ability to bind new information together in memory.

Reversal learning deficits during sleep deprivation: investigating the role of information acquisition failures.

Besides degrading vigilant attention, total sleep deprivation (TSD) impairs reversal learning performance and blunts affective reactions to feedback. Whether these effects are downstream consequences of information acquisition failures from degraded vigilant attention, or distinct from degraded vigilant attention, is unclear. In well-rested individuals we simulated information acquisition failures by masking a portion of trial information in a go/no-go reversal learning task with four conditions: stimulus masking, feedback masking, alternating stimulus/feedback masking, and no-masking control. No condition reproduced the previously documented pattern of TSD effects, suggesting that information acquisition failures cannot fully account for impaired reversal learning and blunted affective reactions during TSD.

Speed/accuracy trade-off in the effects of acute total sleep deprivation on a sustained attention and response inhibition task.

Total sleep deprivation (TSD) is known to impair sustained attention. However, previously reported effects of TSD on response inhibition are mixed. We administered a "stop-signal" variation of the psychomotor vigilance test, which included 25% of trials requiring withholding of a response to assess response inhibition alongside sustained attention. Participants completed the task at baseline and after 34.5 h of wakefulness. Accuracy was not reduced during TSD. However, response times were significantly slower. A speed/accuracy trade-off allowed participants to effectively withhold responses on inhibition trials and conferred resilience of inhibitory control during TSD under conditions of relatively low time pressure.

A dynamic attentional control framework for understanding sleep deprivation effects on cognition.

The cognitive effects of sleep loss are often attributed to compromised functioning of the prefrontal cortex (PFC). However, compromised PFC functioning does not account for well-known effects of sleep deprivation on vigilance. Furthermore, the executive attentional control functions associated with the PFC show considerable variability in the effects of sleep deprivation. Evidence from neuroimaging suggests that sleep deprived people are sometimes able to maintain performance on cognitive tasks by increasing PFC activation of task-relevant circuits and by recruiting new circuits not typically involved in a particular cognitive operation. Still, little is known about how such compensatory processes work on a functional level, or what tradeoffs in processing they may entail. We propose a dynamic attentional control framework to bridge the gap between the evidence on sleep deprived neural circuits and cognitive task performance. We review evidence that shows that the pattern of preserved and compromised task performance can be understood in terms of sleep deprivation's influence on frontostriatal circuitry such that the ability to maintain task-relevant information in the focus of attention is relatively spared but the ability to update task-relevant information in response to changing circumstances is more negatively affected. This framework helps account for why some tasks are more affected by SD than others, and why individual differences in the effects of sleep deprivation are task-specific.

Working memory loads differentially influence frame-induced bias and normative choice in risky decision making.

Risky decision making can be biased by several types of contextual factors-in particular, framing of outcomes. A popular explanation for outcome framing effects is based on presumed affective reactions that contribute to accepting sure gains and avoiding sure losses. Other theories propose that selective weighting of information about gains and losses contributes to framing bias. Prior research on framing bias has focused on preferences rather than on decisions in which choices can be classified as advantageous (correct) or disadvantageous (incorrect) by a normative criterion. The current study used a novel hypothetical risky decision making task offering choices between a sure option and a gamble option. The gamble was advantageous or disadvantageous on different trials based on the normative criterion of expected value. Results showed risk avoidance with a gain frame and risk seeking with a loss frame, comparable to findings when choices involve preferences. We also examined the impact of working memory loads of either non-affective stimuli, most likely to interfere with acquisition of choice information, or affective stimuli, which might influence affective processes contributing to framing. The results were that non-affective working memory load produced the greatest framing magnitude, while affective load produced changes in framing magnitude across trials that varied by valence. In addition, only the non-affective load decreased advantageous choices and reduced the accuracy of answers to knowledge probe questions about the choices. The findings are consistent with the notion that framing effects may arise from cognitive non-engagement with the task, rather than arising by way of affective processes. Affective loads had a limited influence on framing and no reliable impact on choice accuracy or choice knowledge, suggesting that the affective loads influenced the weighting of choice information.

Joint effects of stress and chronic cannabis use on prospective memory.

RATIONALE: Prospective memory pervades our daily lives and failures can have detrimental consequences. This ability to execute delayed intentions may be impacted by stress, yet few studies have examined these effects. Moreover, as many cannabis users report using cannabis to cope with stress, it is important to understand how stress impacts memory in cannabis users. OBJECTIVES: We assessed the effects of acute and chronic stress on prospective memory to examine whether stress differentially impacts prospective memory in cannabis users vs. non-users. METHODS: Forty cannabis users and 42 non-users were assigned an episodic and a habitual prospective memory test before completing either the stress or no stress condition of the Maastricht Acute Stress Test (MAST). Participants were instructed to execute the habitual test during the MAST and the episodic test shortly after the MAST. Chronic stress was measured using the Perceived Stress Scale, and acute stress was measured using subjective ratings and cortisol. RESULTS: There was a main effect of acute stress indicating that stress detrimentally impacted habitual prospective memory performance. Although there was not a significant stress x cannabis interaction, further planned comparisons indicated the habitual prospective memory impairment was selective to cannabis users. There were also significant negative correlations between (i) episodic prospective memory and both subjective stress as well as chronic stress, and (ii) habitual prospective memory and change in subjective stress. CONCLUSIONS: This study is the first to reveal detrimental effects of acute stress on prospective memory performance, which may be exacerbated in cannabis users.

Trait anxiety impairs cognitive flexibility when overcoming a task acquired response and a preexisting bias.

Individuals with high trait anxiety tend to be worse at flexibly adapting goal-directed behavior to meet changing demands relative to those with low trait anxiety. Past research on anxiety and cognitive flexibility has used tasks that involve overcoming a recently acquired rule, strategy, or response pattern after an abrupt change in task requirements (e.g., choice X led to positive outcomes but now leads to negative outcomes). An important limitation of this research is that many decision making situations require overcoming a preexisting bias (e.g., deciding whether to withdraw a historically winning investment that has experienced recent losses). In the present study we examined whether anxiety differences in the ability to overcome an acquired response extend to the ability to overcome a preexisting bias, when the bias produces objectively disadvantageous decisions. High anxiety (n = 78) and low anxiety participants (n = 76) completed a commonly used measure of cognitive flexibility, reversal learning, and a novel Framed Gambling Task that assessed the extent to which they could make advantageous decisions when the normatively correct choice was inconsistent with a preexisting framing bias. High anxiety participants showed the expected diminished reversal learning performance and also had poorer ability to make advantageous choices that were inconsistent with the framing bias. Worse performance in the Framed Gambling Task was not driven by poor knowledge of risk contingencies, because high anxiety participants reported the same explicit knowledge as low anxiety participants. Instead, the results suggest high anxiety is associated with general deficits in resolving interference from prepotent responses.

Catechol-O-methyltransferase (COMT) genotype affects cognitive control during total sleep deprivation.

Adaptive decision making is profoundly impaired by total sleep deprivation (TSD). This suggests that TSD impacts fronto-striatal pathways involved in cognitive control, where dopamine is a key neuromodulator. In the prefrontal cortex (PFC), dopamine is catabolized by the enzyme catechol-O-methyltransferase (COMT). A functional polymorphism (Val158Met) influences COMT's enzymatic activity, resulting in markedly different levels of prefrontal dopamine. We investigated the effect of this polymorphism on adaptive decision making during TSD. Sixty-six healthy young adults participated in one of two in-laboratory studies. After a baseline day, subjects were randomized to either a TSD group (n = 32) with 38 h or 62 h of extended wakefulness or a well-rested control group (n = 34) with 10 h nighttime sleep opportunities. Subjects performed a go/no-go reversal learning (GNGr) task at well-rested baseline and again during TSD or equivalent control. During the task, subjects were required to learn stimulus-response relationships from accuracy feedback. The stimulus-response relationships were reversed halfway through the task, which required subjects to learn the new stimulus-response relationships from accuracy feedback. Performance on the GNGr task was quantified by discriminability (d') between go and no-go stimuli before and after the stimulus-response reversal. GNGr performance did not differ between COMT genotypes when subjects were well-rested. However, TSD exposed a significant vulnerability to adaptive decision making impairment in subjects with the Val allele. Our results indicate that sleep deprivation degrades cognitive control through a fronto-striatal, dopaminergic mechanism.

Age-differences in cognitive flexibility when overcoming a preexisting bias through feedback.

INTRODUCTION: Older adults are often worse than younger adults at adapting to changing situational demands, and this difference is commonly attributed to an age-related decline in acquiring and updating information. Previous research on aging and cognitive flexibility has used measures that require adapting to novel associations learned during a laboratory task (e.g., choice X led to positive outcomes but now leads to negative outcomes). However, in everyday life people must frequently overcome associations based on preexisting beliefs and biases (e.g., you like to eat cake, but your doctor said to limit your sugar intake). The goal of the present study was to examine possible age-differences in overcoming a preexisting bias and determine whether age-related changes in the acquisition and updating of information influence this form of flexibility. METHOD: Older (n = 20) and younger (n = 20) adults completed a novel task in which repeated choices were made between a sure option (gain or loss) and one of two risky options that were initially ambiguous. Optimal performance required overcoming a framing bias toward being risk seeking to avoid a sure loss and risk averse when offered a sure gain. Probe questions assessed knowledge of choice outcomes, while skin conductance assessed physiological reactions to choices and choice outcomes. RESULTS: Both older and younger adults demonstrated flexibility by reducing the impact of bias over trials, but younger adults had better performance overall. Age-differences were associated with distinct aspects of processing. Young adults had more precise knowledge of choice outcomes and developed skin conductance responses in anticipation of bad choices that were not apparent in older adults. CONCLUSIONS: Older adults showed significant improvement over trials in their ability to decrease bias-driven choices, but younger showed greater flexibility. Age-differences in task performance were based on differences in learning and corresponding representations of task-relevant information.

Sleep Deprivation Diminishes Attentional Control Effectiveness and Impairs Flexible Adaptation to Changing Conditions.

Insufficient sleep is a global public health problem resulting in catastrophic accidents, increased mortality, and hundreds of billions of dollars in lost productivity. Yet the effect of sleep deprivation (SD) on decision making and performance is often underestimated by fatigued individuals and is only beginning to be understood by scientists. The deleterious impact of SD is frequently attributed to lapses in vigilant attention, but this account fails to explain many SD-related problems, such as loss of situational awareness and perseveration. Using a laboratory study protocol, we show that SD individuals can maintain information in the focus of attention and anticipate likely correct responses, but their use of such a top-down attentional strategy is less effective at preventing errors caused by competing responses. Moreover, when the task environment requires flexibility, performance under SD suffers dramatically. The impairment in flexible shifting of attentional control we observed is distinct from lapses in vigilant attention, as corroborated by the specificity of the influence of a genetic biomarker, the dopaminergic polymorphism DRD2 C957T. Reduced effectiveness of top-down attentional control under SD, especially when conditions require flexibility, helps to explain maladaptive performance that is not readily explained by lapses in vigilant attention.

Altered attentional control strategies but spared executive functioning in chronic cannabis users.

BACKGROUND: Cannabis use has increased rapidly in recent decades. The increase in cannabis use makes it important to understand the potential influence of chronic use on attentional control and other executive functions (EFs). Because cannabis is often used to reduce stress, and because stress can constrain attentional control and EFs, the primary goal of this study was to determine the joint effect of acute stress and chronic cannabis use on specific EFs. METHODS: Thirty-nine cannabis users and 40 non-users were assigned to either a stress or no stress version of the Maastricht Acute Stress Test. Participants then completed two cognitive tasks that involve EFs: (1) task switching, and (2) a novel Flexible Attentional Control Task. These two tasks provided assessments of vigilant attention, inhibitory control, top-down attentional control, and cognitive flexibility. Salivary cortisol was assessed throughout the study. RESULTS: Reaction time indices showed an interaction between stress and cannabis use on top-down attentional control (p=0.036, np2=0.059). Follow-up tests showed that cannabis users relied less on top-down attentional control than did non-users in the no stress version. Despite not relying on top-down control, the cannabis users showed no overall performance deficits on the tasks. CONCLUSIONS: Chronic cannabis users performed cognitive tasks involving EFs as well as non-users while not employing cognitive control processes that are typical for such tasks. These results indicate alterations in cognitive processing in cannabis users, but such alterations do not necessarily lead to global performance deficits.

Blunted stress reactivity in chronic cannabis users.

RATIONALE: One of the most commonly cited reasons for chronic cannabis use is to cope with stress. Consistent with this, cannabis users have shown reduced emotional arousal and dampened stress reactivity in response to negative imagery. OBJECTIVES: To our knowledge, the present study represents the first to examine the effects of an acute stress manipulation on subjective stress and salivary cortisol in chronic cannabis users compared to non-users. METHODS: Forty cannabis users and 42 non-users were randomly assigned to complete either the stress or no stress conditions of the Maastricht Acute Stress Test (MAST). The stress condition of the MAST manipulates both physiological (placing hand in ice bath) and psychosocial stress (performing math under conditions of social evaluation). Participants gave baseline subjective stress ratings before, during, and after the stress manipulation. Cortisol was measured from saliva samples obtained before and after the stress manipulation. Further, cannabis cravings and symptoms of withdrawal were measured. RESULTS: Subjective stress ratings and cortisol levels were significantly higher in non-users in the stress condition relative to non-users in the no stress condition. In contrast, cannabis users demonstrated blunted stress reactivity; specifically, they showed no increase in cortisol and a significantly smaller increase in subjective stress ratings. The stress manipulation had no impact on cannabis users' self-reported cravings or withdrawal symptoms. CONCLUSION: Chronic cannabis use is associated with blunted stress reactivity. Future research is needed to determine whether this helps to confer resiliency or vulnerability to stress-related psychopathology as well as the mechanisms underlying this effect.

Feedback Blunting: Total Sleep Deprivation Impairs Decision Making that Requires Updating Based on Feedback.

STUDY OBJECTIVES: To better understand the sometimes catastrophic effects of sleep loss on naturalistic decision making, we investigated effects of sleep deprivation on decision making in a reversal learning paradigm requiring acquisition and updating of information based on outcome feedback. DESIGN: Subjects were randomized to a sleep deprivation or control condition, with performance testing at baseline, after 2 nights of total sleep deprivation (or rested control), and following 2 nights of recovery sleep. Subjects performed a decision task involving initial learning of go and no go response sets followed by unannounced reversal of contingencies, requiring use of outcome feedback for decisions. A working memory scanning task and psychomotor vigilance test were also administered. SETTING: Six consecutive days and nights in a controlled laboratory environment with continuous behavioral monitoring. SUBJECTS: Twenty-six subjects (22-40 y of age; 10 women). INTERVENTIONS: Thirteen subjects were randomized to a 62-h total sleep deprivation condition; the others were controls. MEASUREMENTS AND RESULTS: Unlike controls, sleep deprived subjects had difficulty with initial learning of go and no go stimuli sets and had profound impairment adapting to reversal. Skin conductance responses to outcome feedback were diminished, indicating blunted affective reactions to feedback accompanying sleep deprivation. Working memory scanning performance was not significantly affected by sleep deprivation. And although sleep deprived subjects showed expected attentional lapses, these could not account for impairments in reversal learning decision making. CONCLUSIONS: Sleep deprivation is particularly problematic for decision making involving uncertainty and unexpected change. Blunted reactions to feedback while sleep deprived underlie failures to adapt to uncertainty and changing contingencies. Thus, an error may register, but with diminished effect because of reduced affective valence of the feedback or because the feedback is not cognitively bound with the choice. This has important implications for understanding and managing sleep loss-induced cognitive impairment in emergency response, disaster management, military operations, and other dynamic real-world settings with uncertain outcomes and imperfect information.

Deconstructing and reconstructing cognitive performance in sleep deprivation.

Mitigation of cognitive impairment due to sleep deprivation in operational settings is critical for safety and productivity. Achievements in this area are hampered by limited knowledge about the effects of sleep loss on actual job tasks. Sleep deprivation has different effects on different cognitive performance tasks, but the mechanisms behind this task-specificity are poorly understood. In this context it is important to recognize that cognitive performance is not a unitary process, but involves a number of component processes. There is emerging evidence that these component processes are differentially affected by sleep loss. Experiments have been conducted to decompose sleep-deprived performance into underlying cognitive processes using cognitive-behavioral, neuroimaging and cognitive modeling techniques. Furthermore, computational modeling in cognitive architectures has been employed to simulate sleep-deprived cognitive performance on the basis of the constituent cognitive processes. These efforts are beginning to enable quantitative prediction of the effects of sleep deprivation across different task contexts. This paper reviews a rapidly evolving area of research, and outlines a theoretical framework in which the effects of sleep loss on cognition may be understood from the deficits in the underlying neurobiology to the applied consequences in real-world job tasks.