Abstract
Sleep deprivation is known to have adverse effects on various cognitive abilities. In particular, a lack of sleep has been reported to disrupt memory consolidation and cognitive control functions. Here, focusing on long-term memory and cognitive control processes, we review the consistency and reliability of the results of previous studies of sleep deprivation effects on behavioral performance with variations in the types of stimuli and tasks. Moreover, we examine neural response changes related to these behavioral changes induced by sleep deprivation based on human fMRI studies to determine the brain regions in which neural responses increase or decrease as a consequence of sleep deprivation. Additionally, we discuss about the possibility that light as an environmentally influential factor affects our sleep cycles and related cognitive processes.
Introduction
As indoor lifestyles dominate and the variability of active hours increases, our daily sleep schedule becomes less dependent on environmental cues such as sunlight. For example, a substantial number of people work day and night shifts, such as a nurse’s night shift. In such cases, sleep deprivation can be induced due to a disturbance in the circadian rhythm (Dijk et al., 1997; Hou et al., 2019). In addition, jet lag from air travel or internal emotional states such as excessive stress can also cause sleep deprivation (Weingarten and Collop, 2013). Here, sleep deprivation indicates getting less than the required amount of sleep, which typically between 7 and 9 h of sleep per night for adults (Hirshkowitz et al., 2015). Sleep deprivation can occur for short periods of time, such as 1 day (acute sleep deprivation), or for long periods, such as a few months or longer (chronic sleep deprivation) (Sateia, 2014). Sleep deprivation not only involves physiological changes throughout the entire body but is also considered to be critically related to the decline of a range of cognitive functions (Durmer et al., 2005; Ratcliff and van Dongen, 2009; Jackson et al., 2013; Lo et al., 2016). Moreover, causal relationships between sleep loss and mental disorders, including ADHD, depression, bipolar disorder, and schizophrenia, have been reported (Harvey et al., 2005; Murray and Harvey, 2010; Baird et al., 2012; Wulff et al., 2012; Roberts and Duong, 2014; Yu et al., 2016).
Over the past few decades, there has been a great deal of research on the effects of sleep deprivation on various cognitive functions (Krause et al., 2017). One of the most commonly reported cognitive functions affected by sleep is the memory function (Abel et al., 2013). In particular, it has been suggested that there are critical processes for memory consolidation during slow wave sleep (SWS, Stage 3 and 4) (Plihal and Born, 1997; Rasch et al., 2007; Walker, 2009; Born, 2010; Antony et al., 2012; Cox et al., 2012) or the rapid eye movement (REM) (Plihal and Born, 1997; Wagner et al., 2001; Hornung et al., 2007; Rasch and Born, 2013; Boyce et al., 2016) sleep stage, leading to long-term memory (LTM) formation. Although the distinctive role of each sleep stage is still controversial, cortical activity during those stages of sleep is proposed to be associated with the replay or reinstatement process of experiences to strengthen memories (Pennartz et al., 2002; Paller and Voss, 2004; Antony et al., 2012; Schreiner and Rasch, 2017). Moreover, sleep deprivation has been found to be related to the impairment of various types of LTM formation and to decreases of retrieval performance (Stickgold et al., 2000a; Walker et al., 2002; Korman et al., 2003; Drosopoulos et al., 2005; Gais et al., 2006; van der Helm et al., 2011; Griessenberger et al., 2012). The cognitive control process is also known to be influenced by sleep deprivation (Krause et al., 2017). The overall arousal level is decreased after sleep deprivation, and the corresponding changes usually cause declines in cognitive control functions such as attention and working memory processes (Chee and Choo, 2004; Versace et al., 2006; Kuriyama et al., 2008; Chee et al., 2010).
In this review, we focus on prior human research that addresses the influence of sleep deprivation on long-term memory and cognitive control processes. We used Google Scholar and PubMed to search the literature containing the main keywords “sleep deprivation,” “human,” and “long-term memory (or working memory or executive/cognitive control)” since 2000, and selected papers that report changes in human behaviors and neural responses before and after sleep deprivation. Most of these studies have focused on the effects of acute sleep deprivation rather than chronic sleep deprivation.
In the first and second sections, we summarize behavioral changes and neuronal changes induced by sleep deprivation, which are commonly reported across prior studies despite the use of various types of stimuli and task paradigms. In addition, we discuss influential factors affecting sleep and related cognitive functions.
Long-Term Memory and Sleep Deprivation
Long-term memory (LTM) paradigms usually involve more than 1 day of sleep between learning and retrieval. The beneficial effects of sleep on LTM were found in the early 20th century, and those studies have been replicated numerous times (Drosopoulos et al., 2005; Gais et al., 2006; Aly and Moscovitch, 2010; van der Helm et al., 2011). Specifically, memory researchers have focused on the role of sleep in the memory consolidation process (Abel et al., 2013). Prior studies suggest that neural activity during slow wave sleep (SWS, Stage 3 and 4) or REM sleep stage is associated with the replay of past experiences, contributing to the consolidation process of memory traces (Pennartz et al., 2002; Paller and Voss, 2004; Antony et al., 2012). Thus, sleep deprivation may adversely affect memory consolidation. Here, we examine the effect of sleep deprivation on declarative memories, in which the hippocampus plays a key role, and on non-declarative memories, where other areas rather than the hippocampus are thought to be critical.
Declarative Memories
The formation and consolidation of declarative memories, including verbal, visual, episodic memories, critically involve hippocampal processes (Tulving and Markowitsch, 1998; Eichenbaum, 1999, 2004; Manns and Eichenbaum, 2006). Sleep studies have shown hippocampal reactivation in the form of sharp wave ripples during sleep, which is thought to be critically associated with memory consolidation (Ji and Wilson, 2007; Eschenko et al., 2008; Ramadan et al., 2009; Born, 2010; Diekelmann and Diekelmann and Born, 2010). Therefore, it is expected that sleep deprivation will negatively affect hippocampus-dependent consolidation processes for declarative memories during sleep.
Numerous studies of the effects of sleep deprivation on declarative memory used verbal memory paradigms (Drosopoulos et al., 2005; Gais et al., 2006; Ellenbogen et al., 2009; Feld et al., 2016) (Table 1). Verbal stimuli such as words or nonsense syllables are useful for controlling the variability between stimuli and for generating false memories based on semantic contents. Sleep deprivation has been found to reduce memory performance in simple word recognition tasks (Drosopoulos et al., 2005). Other studies used word pairs to test memory function and showed similar decreases in sleep deprived groups (Gais et al., 2006; Ellenbogen et al., 2009; Feld et al., 2016). Some sleep deprivation studies used a semantically related word list, as in the Deese-Roediger-McDermott (DRM) paradigm to generate false memories. They found that sleep deprivation not only reduces correct trials but also increases false alarm trials (Diekelmann et al., 2008; Fenn et al., 2009). Additionally, Ellenbogen et al. found that sleep deprivation makes memory vulnerable to post-learning interference (Ellenbogen et al., 2009).
TABLE 1
| References | Stimuli | Number of stimuli | N | Comparison/Sleep-deprivation condition | Results | |
| Verbal memory | Drosopoulos et al. (2005) | Word | 96 words | 24 | Sleep vs. Wake /3 h deprivation | Accuracy: sleep > wake, early > late |
| Ellenbogen et al. (2009) | Word pair | 60 pairs | 45 | Sleep vs. Wake /12 h deprivation | Accuracy: sleep > wake | |
| Feld et al. (2016) | Word pair | 160/320 pairs | 101 | Sleep vs. Wake /8 h deprivation | Accuracy: sleep > wake (160 pairs) | |
| Gais et al. (2006) | Word pair | 24 pairs | 14 | Sleep vs. Wake /12 h deprivation | Accuracy: sleep > wake | |
| Diekelmann et al. (2008) | Word (DRM) | 270 words | 43 | Sleep vs. Wake /9 or 33 h deprivation | False memory: sleep < wake (9 h), sleep < wake (33 h) | |
| Fenn et al. (2009) | Word (DRM) | 240 words | 46 | Sleep vs. Wake /12 h deprivation | False memory: sleep < wake | |
| Payne et al. (2009) | Word (DRM) | 120 words | 84 | Sleep vs. Wake /12 h deprivation | Accuracy: sleep > wake | |
| Lutz et al. (2017) | Abstract shape (DRM) | 160 shapes | 16 | Sleep vs. Wake /10 h deprivation | Confidence: sleep > wake | |
| Non-verbal memory | Prehn-Kristensen et al. (2009) | IAPS image | 120 images | 20 | Sleep vs. Wake /11 h deprivation | Accuracy: sleep > wake |
| Rauchs et al. (2004) | Sequence and Location of words | 14 words | 61 | Sleep vs. Wake /4 h deprivation | Accuracy: sleep > REM deprivation | |
| Drosopoulos et al. (2007) | Sequence of words | 32 words | 28 | Sleep vs. Wake /9 h deprivation | Accuracy: sleep > wake | |
| Aly and Moscovitch (2010) | Short-stories | 2 stories | 22 | Sleep vs. Wake /12 h deprivation | Accuracy: sleep > wake | |
| Griessenberger et al. (2012) | Picture sequence | 8 sequences | 34 | Sleep vs. Wake /24 h deprivation | Accuracy: sleep > wake |
Studies of the effects of sleep deprivation on declarative memories.
DRM, Deese-Roediger-McDermott paradigm; IAPS, International Affective Picture System; h, hours.
Other studies based on visual memory paradigms, in which participants memorize abstract shapes or pictures, also revealed lower performance in a sleep-derivation group compared to a group with a normal amount of sleep (Prehn-Kristensen et al., 2009; Lutz et al., 2017). Episodic memory studies have also shown negative effects of sleep deprivation on memory performance (van der Helm et al., 2011; Inostroza and Born, 2013; Tempesta et al., 2017; Chai et al., 2020). Sleep deprivation disrupts the formation of temporal information for both verbal and visual stimuli (Rauchs et al., 2004; Drosopoulos et al., 2007; Griessenberger et al., 2012). Moreover, van der Helm et al. showed that contextual memory was specifically impaired in a sleep-deprivation group even when verbal item memory remained intact (van der Helm et al., 2011).
While most studies of the effect of sleep deprivation on memory address the effects of overnight-sleep deprivation, there is also evidence supporting that 3–4 h-sleep restriction can also affect memory performance (Rauchs et al., 2004; Drosopoulos et al., 2005). Thus, even partial sleep deprivation can affect memory formation and subsequent retrieval.
Non-declarative Memories
Non-declarative memory, often referred to as implicit memory, is an unconscious form of memory that is typically manifested in an automatic manner (Squire and Zola, 1996). Procedural memory, including motor memory and perceptual skills, is one of the most common forms of non-declarative memory. Such memories are known to be associated with neural substrates distinct from those of declarative memories and are thus usually residual, even in patients with amnesic disease or hippocampal lesions (Cohen and Squire, 1980; Döhring et al., 2017; Corkin, 2022). It is known that regions other than the hippocampus, such as cerebellum and striatum, are mainly involved in non-declarative memory processes (Squire and Zola, 1996; Doyon et al., 1997, 2003).
Motor memory refers to memory involving motor skills, such as playing an instrument. In many motor memory tasks, memory performance is evaluated based on sequential finger tapping movements. Studies of sleep deprivation using this finger tapping paradigm have found that performance decreases in a sleep-deprived condition (Walker et al., 2002; Korman et al., 2003; Debas et al., 2010) (Table 2). In addition, Korman et al. showed that sleep enhances resistance to post-learning interference tasks such as inverse-tapping-sequence learning. Another study also found a motor memory decline after sleep deprivation based on the mirror task paradigm, in which participants were asked to trace drawings by looking in a mirror to observe a picture to be traced.
TABLE 2
| References | Task type | Stimuli | N | Comparison/Sleep-deprivation condition | Results | |
| Motor memory | Walker et al. (2002) | Finger tapping task | 5 element sequence | 62 | Sleep vs. Wake /12 h deprivation | Accuracy: sleep > wake |
| Korman et al. (2003) | Finger tapping task | 5 element sequence | 83 | Sleep vs. Wake /12 h deprivation | Accuracy: sleep > wake | |
| Debas et al. (2010) | Finger tapping task | 5 element sequence | 48 | Sleep vs. Wake /12 h deprivation | Accuracy: sleep > wake | |
| Perceptual memory | Aeschbach et al. (2008) | Visual texture discrimination task | T and L | 16 | Sleep vs. Disruption /4 h deprivation | Accuracy: sleep > disruption |
| Stickgold et al. (2000b) | Visual texture discrimination task | T and L | 57 | Sleep vs. Wake /8 or 12 h deprivation | Accuracy: sleep > wake | |
| Stickgold et al. (2000a) | Visual texture discrimination task | T and L | 11 | Sleep vs. Wake /24 h deprivation | Accuracy: sleep > wake | |
| Mascetti et al. (2013) | Visual orientation discrimination task | Grating | 32 | Sleep vs. Wake /12 h deprivation | Accuracy: sleep > wake |
Studies of the effects of sleep deprivation on non-declarative memories.
h, hours.
Prior studies based on perceptual skill memory paradigms, mostly visual discrimination tasks, have also shown reduced performance outcomes under a sleep-deprived condition (Stickgold et al., 2000a,b; Aeschbach et al., 2008; Mascetti et al., 2013). Notably, perceptual skill memory has been shown to decline simply after disrupting sleep quality with the same amount of total sleep time (Aeschbach et al., 2008) (Table 2). Moreover, as with declarative memory, relatively short durations of sleep deprivation also affect the procedural memory performance outcomes (Aeschbach et al., 2008).
These results indicate that not only declarative memories but also various types of non-declarative memories are negatively affected by sleep deprivation, despite the fact that these memories are known to depend less on hippocampal consolidation (Döhring et al., 2017; Corkin, 2022). In sum, sleep deprivation adversely affects our overall memory performance, including both declarative and non-declarative memory processes.
Cognitive Control and Sleep Deprivation
Cognitive control (or executive control) is also known to be especially susceptible to sleep deprivation (Krause et al., 2017). Previous studies have found that sleep deprivation also negatively affects cognitive control processes (Table 3). Sleep-related changes in cognitive control are important because such changes can affect our overall goal-dependent behaviors (Paxton et al., 2008; Braver, 2012; Nathan Spreng et al., 2014). In this section, we focus on the effects of sleep deprivation on working memory and attention processes.
TABLE 3
| References | Task type | Stimuli | N | Comparison/ Sleep-deprivation condition | Results | |
| Working memory | Chee and Choo (2004) | Delayed match-to-sample | Alphabet letter | 14 | Sleep vs. Wake /24 h deprivation | Accuracy: sleep > wake |
| Mu et al. (2005a) | Delayed match-to-sample | Alphabet letter | 33 | Sleep vs. Wake /30 h deprivation | Reaction time: sleep < wake Accuracy: sleep > wake | |
| Luber et al. (2008) | Delayed match-to-sample | Alphabet letter | 15 | Sleep vs. Wake /57 h deprivation | Reaction time: sleep < wake | |
| Drummond et al. (2012) | Delayed match-to-sample | Color | 44 | Sleep vs. Partial sleep vs. Wake /4 or 24 h deprivation | No difference | |
| Xie et al. (2019) | Delayed match-to-sample | Color | 110 | Sleep quality | Positive correlation between sleep quality and WM performance | |
| Kuriyama et al. (2008) | N-back task | Button image | 29 | Sleep vs. Wake /10 h deprivation | WM capacity: sleep > wake | |
| Gradisar et al. (2008) | Delayed recall | Word | 143 | Sleep vs. Restricted sleep /8 h sleep restriction | Accuracy: restricted sleep < sleep | |
| Attention | Mander et al. (2008) | Spatial attention task | Orientation | 7 | Sleep vs. Wake /36 h deprivation | Commission error: no difference Omission error: sleep < wake |
| Versace et al. (2006) | Spatial attention task | Orientation | 14 | Sleep vs. Restricted sleep /5 h sleep restriction | Reaction time: sleep < restricted sleep (invalid cue) | |
| Bocca and Denise (2006) | Saccade task | Dots | 10 | Sleep vs. Wake /24 h deprivation | Latency: sleep < wake | |
| Chee et al. (2010) | Object-selective attention task | Scene, face stimuli | 26 | Sleep vs. Wake /24 h deprivation | Reaction time: sleep < wake, Accuracy: sleep > wake, | |
| Jennings et al. (2003) | Go/No-Go task | Orientation | 20 | Sleep vs. Wake /12 h deprivation | Reaction time: sleep < wake Accuracy: sleep > wake (incompatible cue) | |
| Nota and Coles (2018) | Attention disengagement task | Emotional images | 52 | Sleep duration | Shorter sleep duration correlated with slower disengaging from negative stimuli | |
| Fallone et al. (2001) | The child attention profile | Questionnaire | 82 | Sleep vs. Restricted sleep /6 h sleep restriction | Inattentive behavior: restricted sleep > sleep |
Studies of the effects of sleep deprivation on cognitive control processes.
WM, working memory; h, hours.
Working Memory
Working memory is a cognitive ability that allows one to hold information temporarily to guide current behavior (Baddeley and Hitch, 1974; Lee and Baker, 2016). The delayed match-to-sample (DMTS) task is the most widely used paradigm to test working memory. In prior verbal working memory studies based on DMTS, sleep deprivation generally decreases accuracy levels and increases reaction times (Chee and Choo, 2004; Mu et al., 2005a; Luber et al., 2008). However, in visual working memory studies, discrepancies were reported with regard to the effects of sleep deprivation. While some studies show a performance decline after sleep deprivation (Xie et al., 2019), others show no differences between sleep and waking conditions (Drummond et al., 2012). In addition, MacDonald et al. reported a temporal difference in the effect of sleep deprivation; no group difference was found in the early phase of the working memory task, while a performance decline in a sleep-deprived group was found in the late phase of the task (MacDonald et al., 2018). Because working memory may be mainly affected by increased fatigue or the altered brain states induced by sleep deprivation, momentary focusing may compensate for the decline of performance from sleep deprivation. Consistent with this idea, some studies reported no differences between groups assessed on difficult or complex task conditions which involve intentional effort (Chee and Choo, 2004; Mu et al., 2005a). Thus, it may be possible that the effect of sleep deprivation on working memory depends on the balance or interaction between the attention process and sleep-deprivation-induced changes.
Attention
Sleep-deprivation effects have been reported in various attention studies. Bocca and Denise used a simple saccade task to evaluate sustained attention and found longer latency times in a sleep-deprived group (Bocca and Denise, 2006). On a selective-attention task requiring high top-down regulation, performance declines in sleep-deprived groups with an orientation cue (Jennings et al., 2003; Versace et al., 2006; Mander et al., 2008), and an object cue (Chee et al., 2010). Furthermore, performance changes during attention processing were found to occur even with differences in short and long sleep durations (Fallone et al., 2001; Versace et al., 2006). Additionally, there are numerous reports of sleep deprivation effects, especially when inhibitory top-down control is required (Jennings et al., 2003; Versace et al., 2006; Mander et al., 2008; Nota and Coles, 2018).
Taken together, these studies mostly suggest sleep-deprivation-induced declines in the performance outcomes of cognitive control processes. However, compared to the effects on long-term memory, the effects of sleep deprivation on the cognitive control process depend more sensitively on the experimental conditions.
Neural Response Changes Induced by Sleep Deprivation
The aforementioned studies suggest that sleep deprivation induces declines in memory and executive control performances in common, despite the different task paradigms utilized. This leads to the question of what neural bases underlie the cognitive decline induced by sleep deprivation. In this section, we focused on human fMRI studies that investigated the effects of sleep deprivation on memory and executive control processes. Sleep-derivation associated activity changes were commonly observed in the prefrontal cortex, parietal lobe, hippocampus, and basal ganglia/thalamus.
Prefrontal Cortex
Changes of neural responses in the prefrontal cortex are reliably observed in the human fMRI literatures (Table 4). In the lateral prefrontal areas, including the dorsolateral prefrontal cortex (dlPFC) and ventrolateral prefrontal cortex (vlPFC), decreased neural responses as a result of sleep deprivation have often been reported (Mu et al., 2005b; Lythe et al., 2012; Wang et al., 2016). In some studies, sleep-loss-associated increases in activity in the dlPFC were also reported (Chee and Choo, 2004; Beebe et al., 2009; Drummond et al., 2012). Consistent with the fact that the PFC regions are mainly involved in working memory, attention and executive control processes (Wagner et al., 2001; Curtis and D’Esposito, 2003; Barbey et al., 2013), the response changes in the PFC as a consequence of sleep deprivation were mostly observed in the studies using working memory tasks (Mu et al., 2005b; Chee et al., 2006; Lythe et al., 2012) (Table 4).
TABLE 4
| References | Sleep deprivation | Cognitive process | N | Neural response changes | |
| Decrease | Increase | ||||
| Drummond et al. (2000) | 35 h deprivation | Short-term verbal memory task | 13 | Temporal lobe | PFC, parietal lobe |
| Habeck et al. (2004) | 48 h deprivation | Working memory task | 18 | Parietal, temporal, occipital lobe | Cerebellum, basal ganglia, thalamus, Anterior cingulate cortex (ACC) |
| Bell-McGinty et al. (2004) | 48 h deprivation | Short-term non-verbal memory task | 19 | Bilateral posterior cerebellum, right fusiform gyrus, precuneus, left lingual and inferior temporal gyri | Bilateral insula, claustrum, tight putamen |
| Chee and Choo (2004) | 24 h deprivation | Working memory task | 14 | Anterior medial frontal, left posterior cingulate, medial parietal region | Dorsal lateral prefrontal cortex (dlPFC) |
| Mu et al. (2005b) | 30 h deprivation | Working memory task | 20 | Left posterior parietal cortex (PPC), left ventro lateral prefrontal cortex (vlPFC), right inferior PPC, right dlPFC | |
| Chee et al. (2006) | 24 h, 35 h deprivation | Working memory task | 26 | Left lPFC, ACC, bilateral superior parietal region, left thalamus | |
| Lim et al. (2007) | 24 h deprivation | Working memory task | 19 | Bilateral parietal region | |
| Gais et al. (2007) | 24 h deprivation | Long-term verbal memory task | 18 | Hippocampus (HPC) | |
| Yoo et al. (2007) | 35 h deprivation | Long-term episodic memory task | 28 | Bilateral posterior HPC | |
| Chee and Chuah (2007) | 24 h deprivation | Working memory task | 30 | Precuneus, temporoparietal junction (TPJ) | |
| Beebe et al. (2009) | Chronic deprivation | Working memory task | 6 | Left postcentral gyrus, lingual gyrus, ACC, middle frontal gyrus (MFG), PCC, parahippocampal gyrus, fusiform gyrus, superior temporal gyrus, middle temporal gyrus | Precuneus, premotor, dlPFC, insula, inferior parietal lobe (IPL), cingulate gyrus |
| Van Der Werf et al. (2009) | Disturbed sleep | Long-term visual memory task | 13 | Anterior HPC | |
| Gujar et al. (2010) | 36 h deprivation | Attention task | 28 | Precuneus | Dorsal ACC |
| Lim et al. (2010) | 24 h deprivation | Attention task | 23 | Left inferior frontal cortex, left intraparietal sulcus (IPS) | |
| Jackson et al. (2011) | 27 h deprivation | Attention task | 12 | Left superior frontal gyrus | |
| Gujar et al. (2011) | 32 h deprivation | Attention task | 27 | right posterior hippocampus, precuneus, left middle occipital gyrus | Ventral tegmental area (VTA), left putamen, amygdala, left insula |
| Libedinsky et al. (2011) | 24 h deprivation | Attention task | 22 | Ventro medial PFC (vmPFC) | |
| Rosales-Lagarde et al. (2012) | REM/NREM sleep deprivation | Emotion reactivity task | 20 | NREM: right inferior, middle frontal gyri, right fusiform gyrus, left superior frontal gyrus, inferior parietal lobe, posterior middle temporal gyrus, parahippocampal gyrus REM: left anterior, posterior cingulate gyri, left posterior middle temporal gyrus | REM: left middle occipital gyrus |
| Lythe et al. (2012) | 31 h deprivation | Working memory task | 20 | High-load WM: right vlPFC | Low-load WM: Right inferior parietal lobe |
| Dai et al. (2015) | 72 h deprivation | Attention task | 12 | left IPL | |
| Wang et al. (2016) | 24 h deprivation | Attention task | 16 | Putamen, claustrum, MFG, IPL | Cuneus |
| Sterpenich et al. (2017) | 24 h deprivation | Verbal memory task, Verbal decision task | 30 | HPC, middle occipital gyrus, Precuneus | |
| Nir et al. (2017) | Full night sleep deprivation | Face/non-face categorization psychomotor vigilance task (cognitive lapses) | 12 | Medial temporal lobe (MTL) spike responses are attenuated, delayed and lengthened | |
| Chen et al. (2018) | 24 h deprivation | Attention network task | 16 | Right cerebellum anterior lobe | Inferior occipital gyrus, left thalamus, insula, postcentral gyrus |
| Zhao et al. (2019) | 24 h deprivation | Stop-signal task | 22 | Inferior frontal gyrus, MFG, Supplementary motor area, insula, ACC, Midcingulate cortex, Lingual gyrus, occipital cortex, fusiform gyrus, superior parietal lobule, IPL, supramarginal gyrus, Angular gyrus, Thalamus, Temporal gyrus, Subthalamic nucleus | |
Human fMRI studies of the effects of sleep deprivation on neural response changes.
WM, working memory; REM, Rapid eye movement sleep; NREM, non-rapid eye movement sleep; h, hours.
Parietal Lobe
Regions in the parietal lobe were also frequently linked to sleep-deprivation-induced changes in fMRI responses (Table 4). Although a few studies suggest increased neural responses under sleep-deprived conditions (Drummond et al., 2012; Lythe et al., 2012; Wang et al., 2016), most studies showed that sleep deprivation induces a reduction of neural responses in the parietal regions during cognitive tasks (Bell-McGinty et al., 2004; Habeck et al., 2004; Ninad et al., 2010; Dai et al., 2015). Specifically, sleep-loss-induced changes in the inferior parietal lobe (IPL) and the precuneus have been reliably reported. The IPL is considered to play an important role in various cognitive processes, such as spatial attention, semantic memory, and social cognition (Numssen et al., 2020). The precuneus is involved in various cognitive functions, such as episodic memory retrieval as a functional core of the default-mode network (Cavanna and Trimble, 2006; Utevsky et al., 2014). Sleep deprivation effects in these regions were observed in various cognitive processes, especially in working memory/cognitive control processes.
Hippocampus
Neural response changes in the hippocampus have mainly been reported in long-term memory studies that utilize sleep-deprivation conditions (Gais et al., 2007; Yoo et al., 2007; Van Der Werf et al., 2009; Sterpenich et al., 2017). As noted earlier, although sleep deprivation affects memory function mainly by disrupting the memory consolidation process, behavioral changes of non-hippocampus-dependent memory indicate a negative effect of sleep deprivation on the encoding or retrieval phase.
Human fMRI studies show reductions in the neural responses of the hippocampus during memory encoding or retrieval after sleep deprivation (Gais et al., 2007; Yoo et al., 2007; Van Der Werf et al., 2009; Sterpenich et al., 2017). In addition, neural attenuation at the single neuron level was also found in the medial temporal lobe (Nir et al., 2017). One possible interpretation of the reduced neural response in the hippocampus during retrieval may be a reflection of the negative effect of sleep deprivation on memory consolidation.
Basal Ganglia/Thalamus
While sleep deprivation is mainly associated with decreases in neural responses in the prefrontal, parietal, and hippocampal regions, increased responses under sleep-deprived conditions have mainly been reported in the basal ganglia and thalamus. This opposite direction in the neural response change in these regions can be interpreted in two ways. First, these regions are hyperactivated by extended sleep deprivation itself and irrelevant to cognitive functions. In particular, the thalamus is involved in consciousness and modulation of the sleep and wake cycle (Steriade and Llinas, 1988; Redinbaugh et al., 2020). Therefore, increased sleepiness and fatigue could require more activity to sustain consciousness. Second, this hyperactivity could be a compensatory process. Given that other regions show decreased activity after sleep deprivation, the basal ganglia and thalamus, regions which are less affected by sleep deprivation, could compensate for the lack of required neural responses.
Influential Factors Affecting Sleep and Related Cognitive Functions
Sleep Regulation by Homeostatic and Circadian Processes
Prior sleep studies suggest that sleep is regulated by two basic processes: a homeostatic process and a circadian process. As mentioned in the introduction, sleep deprivation can be caused by experiences such as jet lag from air travel or stressful events, which we often experience in modern society. These experiences likely affect our circadian rhythms, which can interact with the homeostatic process.
Sleep is known to show a homeostatic aspect with regard to maintaining sleep amount (Borbely and Wirz-Justice, 1982; Deboer, 2018). Thus, based on this homeostatic process, sleep deprivation or sleep restriction is usually followed by a sleep extension (Arnal et al., 2015). Moreover, EEG studies show that NREM sleep can be deepened to compensate sleep loss (Porkka-Heiskanen, 2013; Ong et al., 2016). Our sleep and wakefulness cycles also depend on endogenous circadian rhythms (Ibuka et al., 1977; Adrien et al., 1991; Åkerstedt, 2003). The suprachiasmatic nuclei (SCN) in the hypothalamus is known to play a key role in this circadian process as the primary pacemaker (Riemersma et al., 2004). This circadian process of the brain is susceptible to external timing cues called zeitgebers. The term zeitgeber (literally, time giver) refers to environmental variables, such as the light/dark cycle, the temperature, and melatonin, which are capable of acting as circadian time cues (Aschoff and Pohl, 1978; Rawashdeh and Maronde, 2012; Heyde and Oster, 2019). The circadian process regulates the timing of sleep while sleep homeostatic process influences mainly on the depth and maintenance of sleep (Deboer, 2018). Despite the fact that homeostatic and circadian processes are able to work independently, sleep models propose that the two types mutually influence each other (Borbély and Achermann, 1999; Huang et al., 2011; Fisher et al., 2013; Borbély et al., 2016). Specifically, one finding supported by strong evidence is that the circadian rhythm is less susceptible to light when the sleep homeostatic pressure is increased (Deboer, 2018). Thus, the quantity and quality of sleep can be determined by the outcome of the interaction between the circadian process and the homeostatic process, leading to different degrees of change in the associated cognitive processing.
Influence of Light on Circadian Rhythms, Sleep, and Related Cognitive Processes
Given that disturbances in the sleep-wake cycle or sleep deprivation adversely affect cognitive functions, including long-term memory and cognitive control processes, as we discussed above (Chee and Choo, 2004; Mander et al., 2008; Ellenbogen et al., 2009; Debas et al., 2010), the modulation of circadian rhythms by controlling zeitgebers is likely to affect our cognitive functions. This modulation may contribute to the recovery of cognitive functions impaired by sleep deprivation. In this section, we discuss this possibility focusing on a powerful zeitgeber, light.
Light or the light/dark cycle is known to be the most powerful zeitgeber. It is known that the projection between retinal ganglion cells, which respond directly to light, and the SCN, which is the anterior part of the hypothalamus and which is responsible for regulating circadian rhythms and melatonin production (Berson et al., 2002; Dijk and Archer, 2009), is critical for synchronization between the circadian rhythms and the day-night cycle. In particular, a subset of mammalian (including human) retinal ganglion cells contains melanopsin, which is a type of photopigment belonging to a family of opsins (Hankins et al., 2008), and melanopsin cells play a key role in the synchronization of the circadian clocks to light, including modulation of sleep and the suppression of pineal melatonin production (Ruby et al., 2002; Tsai et al., 2009; Markwell et al., 2010; Bailes and Lucas, 2013).
Melanopsin photoreceptors are most sensitive to blue light wavelength at around 480 nm (Panda et al., 2005; Duda et al., 2020). Consistent with this, short-wavelength light exposure had the same effect on adjustments (phase shifts) of the human circadian system as white pulses that contained 185-fold more photons (Warman et al., 2003). This result suggests that the human circadian system mainly depends on the effect of short-wavelength light (Warman et al., 2003). In line with this, blue light exposure in the evening has been shown to suppress the evening onset of melatonin and lead to a phase delay of the circadian rhythm (Cajochen et al., 2005, 2011; Chellappa et al., 2011; Alkozei et al., 2016). Moreover, morning exposure to blue light is also known to suppress melatonin and leads to a phase advance of the circadian rhythm (Wright et al., 2004; Lack et al., 2007; Sletten et al., 2009).
We examined these adverse effects of sleep deprivation on cognitive functions. If controlling light exposure alters the circadian rhythm, including our sleep cycle through the connections from the retina to the SCN, subsequent changes of various cognitive functions, including memory and executive control processes, can be expected. Consistent with this expectation, exposure to higher levels of melanopic (short wavelength-enriched) white light was found to be associated with significantly less sleepiness, better working memory, better processing speeds, and better procedural learning outcomes in moderately sleep-restricted adults (Grant et al., 2021).
At present, we are often exposed to artificial light for long time, even at night, and widely used conventional LED lights have particularly strong blue light intensity (Shen et al., 2014). Therefore, disturbances in circadian rhythms and sleep deprivation are likely to be further accelerated under these conditions. Despite the beneficial effects of blue light exposure on working memory performance and alertness outcomes (Cajochen, 2007; Vandewalle et al., 2009; Chellappa et al., 2011; Esaki et al., 2016), there is still a possibility that long-term exposure to high-intensity blue light may cause disturbances in melatonin levels or the sleep cycle, which can lead to sleep deprivation and decreases in related cognitive functions. Recently, there have been efforts to improve this limitation of conventional LEDs. One example is a newly developed LED that mimics the spectrum of daylight (daylight-LED); the blue light intensity is comparable to the intensity levels of light with other wavelength ranges (Cajochen et al., 2019; Grant et al., 2021). By comparing conventional-LED and daylight-LED exposure conditions, Cajochen et al. showed that the daylight-LED has beneficial effects on sleep as well as visual comfort and alertness (Cajochen et al., 2019). Longitudinal studies in the future are needed to clarify whether these efforts based on light-source modulation can contribute to restoring disturbances in the human sleep cycle and the subsequent impairments of cognitive functions such as long-term memory processes.
Conclusion
Prior research of human sleep deprivation generally suggests declines in long-term memory and cognitive control abilities under sleep deprivation conditions. Although the effects of sleep deprivation were tested based on different types of task paradigms and various stimuli, fairly consistent results across the studies thus far pertaining to the changes in behavioral performance outcomes and neural responses have been reported. However, there are still points that must be considered. Although the brain regions and corresponding neural response changes associated with sleep deprivation and related cognitive disruptions have been suggested, it remains still unclear as to how these neuronal changes are caused by sleep deprivation and how they disrupt cognitive processes. In particular, future studies will be needed to elucidate the direct effect of sleep deprivation on the consolidation processes of long-term memory, and to define the interaction mechanism between task difficulty and sleep deprivation considering executive control processes. Further, more in-depth research is needed to clarify the effects of environmental factors inevitably encountered in our everyday lives, such as artificial light, on our sleep and related cognitive processes.
Publisher’s Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Statements
Author contributions
TK, SK, MK, JK, and S-HL wrote the manuscript. TK, SK, and S-HL conceptualized and edited the manuscript. All authors contributed to the article and approved the submitted version.
Funding
This study received funding from Seoul Semiconductor Co. Ltd. The funder was not involved in the study design, collection, analysis, interpretation of data, the writing of this article, or the decision to submit it for publication.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
1
AbelT.HavekesR.SaletinJ. M.WalkerM. P. (2013). Sleep, plasticity and memory from molecules to whole-brain networks.Curr. Biol.23R774–R788. 10.1016/j.cub.2013.07.025
2
AdrienJ.DugovicC.MartinP. (1991). Sleep-wakefulness patterns in the helpless rat.Physiol. Behav.49257–262. 10.1016/0031-9384(91)90041-l
3
AeschbachD.CutlerA. J.RondaJ. M. (2008). A role for non-rapid-eye-movement sleep homeostasis in perceptual learning.J. Neurosci.282766–2772. 10.1523/JNEUROSCI.5548-07.2008
4
ÅkerstedtT. (2003). Shift work and disturbed sleep/wakefulness.Occup. Med. (Chic. Ill).5389–94.
5
AlkozeiA.SmithR.PisnerD. A.VanukJ. R.BerryhillS. M.FridmanA.et al (2016). Exposure to blue light increases subsequent functional activation of the prefrontal cortex during performance of a working memory task.Sleep391671–1680. 10.5665/sleep.6090
6
AlyM.MoscovitchM. (2010). The effects of sleep on episodic memory in older and younger adults.Memory18327–334. 10.1080/09658211003601548
7
AntonyJ. W.GobelE. W.O’HareJ. K.ReberP. J.PallerK. A. (2012). Cued memory reactivation during sleep influences skill learning.Nat. Neurosci.151114–1116. 10.1038/nn.3152
8
ArnalP. J.SauvetF.LegerD.van BeersP.BayonV.BougardC.et al (2015). Benefits of sleep extension on sustained attention and sleep pressure before and during total sleep deprivation and recovery.Sleep381935–1943. 10.5665/sleep.5244
9
AschoffJ.PohlH. (1978). Phase relations between a circadian rhythm and its zeitgeber within the range of entrainment.Naturwissenschaften6580–84. 10.1007/BF00440545
10
BaddeleyA. D.HitchG. (1974). Working memory.Psychol. Learn. Motiv. Adv. Res847–89.
11
BailesH. J.LucasR. J. (2013). Human melanopsin forms a pigment maximally sensitive to blue light (λmax ≈ 479 nm) supporting activation of Gq/11 and Gi/o signalling cascades.Proc. R. Soc. B Biol. Sci.280:20122987. 10.1098/rspb.2012.2987
12
BairdA. L.CooganA. N.SiddiquiA.DonevR. M.ThomeJ. (2012). Adult attention-deficit hyperactivity disorder is associated with alterations in circadian rhythms at the behavioural, endocrine and molecular levels.Mol. Psychiatry17988–995. 10.1038/mp.2011.149
13
BarbeyA. K.KoenigsM.GrafmanJ. (2013). Dorsolateral prefrontal contributions to human working memory.Cortex491195–1205. 10.1016/j.cortex.2012.05.022
14
BeebeD. W.DiFrancescoM. W.TlustosS. J.McNallyK. A.HollandS. K. (2009). Preliminary fMRI findings in experimentally sleep-restricted adolescents engaged in a working memory task.Behav. Brain Funct.51–7. 10.1186/1744-9081-5-9
15
Bell-McGintyS.HabeckC.HiltonH. J.RakitinB.ScarmeasN.ZarahnE.et al (2004). Identification and differential vulnerability of a neural network in sleep deprivation.Cereb. Cortex14496–502. 10.1093/cercor/bhh011
16
BersonD. M.DunnF. A.TakaoM. (2002). Phototransduction by retinal ganglion cells that set the circadian clock.Science2951070–1073. 10.1126/science.1067262
17
BoccaM. L.DeniseP. (2006). Total sleep deprivation effect on disengagement of spatial attention as assessed by saccadic eye movements.Clin. Neurophysiol.117894–899. 10.1016/j.clinph.2006.01.003
18
BorbélyA. A.AchermannP. (1999). Sleep homeostasis and models of sleep regulation.J. Biol. Rhythms14557–568. 10.1177/074873099129000894
19
BorbelyA. A.Wirz-JusticeA. (1982). Sleep, sleep deprivation and depression. a hypothesis derived from a model of sleep regulation.Human Neurobiol.1205–210.
20
BorbélyA. A.DaanS.Wirz-JusticeA.DeboerT. (2016). The two-process model of sleep regulation: a reappraisal.J. Sleep. Res.25131–143. 10.1111/jsr.12371
21
BornJ. (2010). Slow-wave sleep and the consolidation of long-term memory.World J. Biol. Psychiatry1116–21. 10.3109/15622971003637637
22
BoyceR.GlasgowS. D.WilliamsS.AdamantidisA. (2016). Sleep research: Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation.Science352812–816. 10.1126/science.aad5252
23
BraverT. S. (2012). The variable nature of cognitive control: a dual mechanisms framework.Trends Cogn. Sci.16106–113.
24
CajochenC. (2007). Alerting effects of light.Sleep Med. Rev.11453–464.
25
CajochenC.FreyS.AndersD.SpätiJ.BuesM.ProssA.et al (2011). Evening exposure to a light-emitting diodes (LED)-backlit computer screen affects circadian physiology and cognitive performance.J. Appl. Physiol.1101432–1438. 10.1152/japplphysiol.00165.2011
26
CajochenC.FreyburgerM.BasishviliT.GarbazzaC.RudzikF.RenzC.et al (2019). Effect of daylight LED on visual comfort, melatonin, mood, waking performance and sleep.Light. Res. Technol.511044–1062.
27
CajochenC.MünchM.KobialkaS.KräuchiK.SteinerR.OelhafenP.et al (2005). High sensitivity of human melatonin, alertness, thermoregulation, and heart rate to short wavelength light.J. Clin. Endocrinol. Metab.901311–1316. 10.1210/jc.2004-0957
28
CavannaA. E.TrimbleM. R. (2006). The precuneus: A review of its functional anatomy and behavioural correlates.Brain129564–583. 10.1093/brain/awl004
29
ChaiY.FangZ.YangF. N.XuS.DengY.RaineA.et al (2020). Two nights of recovery sleep restores hippocampal connectivity but not episodic memory after total sleep deprivation.Sci. Rep.101–11. 10.1038/s41598-020-65086-x
30
CheeM. W. L.ChooW. C. (2004). Functional imaging of working memory after 24 hr of total sleep deprivation.J. Neurosci.244560–4567. 10.1523/JNEUROSCI.0007-04.2004
31
CheeM. W. L.ChuahY. M. L. (2007). Functional neuroimaging and behavioral correlates of capacity decline in visual short-term memory after sleep deprivation.Proc. Natl. Acad. Sci. U.S.A.1049487–9892. 10.1073/pnas.0610712104
32
CheeM. W. L.ChuahL. Y. M.VenkatramanV.ChanW. Y.PhilipP.DingesD. F. (2006). Functional imaging of working memory following normal sleep and after 24 and 35 h of sleep deprivation: Correlations of fronto-parietal activation with performance.Neuroimage31419–428. 10.1016/j.neuroimage.2005.12.001
33
CheeM. W. L.TanJ. C.ParimalS.ZagorodnovV. (2010). Sleep deprivation and its effects on object-selective attention.Neuroimage491903–1910. 10.1016/j.neuroimage.2009.08.067
34
ChellappaS. L.SteinerR.BlattnerP.OelhafenP.GötzT.CajochenC. (2011). Non-visual effects of light on melatonin, alertness and cognitive performance: can blue-enriched light keep us alert?PLoS One6:e16429. 10.1371/journal.pone.0016429
35
ChenL.QiX.ZhengJ. (2018). Altered regional cortical brain activity in healthy subjects after sleep deprivation: a functional magnetic resonance imaging study.Front. Neurol.9:588. 10.3389/fneur.2018.00588
36
CohenN. J.SquireL. R. (1980). Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that.Science210207–210. 10.1126/science.7414331
37
CorkinS. (2022). What’s new with the amnesic patient H.M.?Nat. Rev. Neurosci.3153–160. 10.1038/nrn726
38
CoxR.HofmanW. F.TalaminiL. M. (2012). Involvement of spindles in memory consolidation is slow wave sleep-specific.Learn. Memory19264–267. 10.1101/lm.026252.112
39
CurtisC. E.D’EspositoM. (2003). Persistent activity in the prefrontal cortex during working memory.Trends Cogn. Sci.7415–423.
40
DaiX. J.LiuC. L.ZhouR. L.GongH. H.WuB.GaoL.et al (2015). Long-term total sleep deprivation decreases the default spontaneous activity and connectivity pattern in healthy male subjects: a resting-state fMRI study.Neuropsychiatr. Dis. Treat.11761–772. 10.2147/NDT.S78335
41
DebasK.CarrierJ.OrbanP.BarakatM.LunguO.VandewalleG.et al (2010). Brain plasticity related to the consolidation of motor sequence learning and motor adaptation.Proc. Natl. Acad. Sci. U S A10717839–17844. 10.1073/pnas.1013176107
42
DeboerT. (2018). Sleep homeostasis and the circadian clock: do the circadian pacemaker and the sleep homeostat influence each other’s functioning?Neurobiol. Sleep Cir. Rhythms568–77. 10.1016/j.nbscr.2018.02.003
43
DiekelmannS.BornJ. (2010). Slow-wave sleep takes the leading role in memory reorganization.Nat. Rev. Neurosci.11:218.
44
DiekelmannS.LandoltH. P.LahlO.BornJ.WagnerU. (2008). Sleep loss produces false memories.PLoS One3:e3512. 10.1371/journal.pone.0003512
45
DijkD. J.ArcherS. N. (2009). Light, sleep, and circadian rhythms: together again.PLoS Biol.7:e1000145. 10.1371/journal.pbio.1000145
46
DijkD. J.ShanahanT. L.DuffyJ. F.RondaJ. M.CzeislerC. A. (1997). Variation of electroencephalographic activity during non-rapid eye movement and rapid eye movement sleep with phase of circadian melatonin rhythm in humans.J. Physiol.505851–858. 10.1111/j.1469-7793.1997.851ba.x
47
DöhringJ.StoldtA.WittK.SchönfeldR.DeuschlG.BornJ.et al (2017). Motor skill learning and offline-changes in TGA patients with acute hippocampal CA1 lesions.Cortex89156–168. 10.1016/j.cortex.2016.10.009
48
DoyonJ.GaudreauD.LaforceR. L.CastonguayM.BédardP. J.BédardF.et al (1997). Role of the striatum, cerebellum, and frontal lobes in the learning of a visuomotor sequence.Brain Cogn.34218–245. 10.1006/brcg.1997.0899
49
DoyonJ.PenhuneV.UngerleiderL. G. (2003). Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning.Neuropsychologia41252–262.
50
DrosopoulosS.WagnerU.BornJ. (2005). Sleep enhances explicit recollection in recognition memory.Learn. Mem.1244–51. 10.1101/lm.83805
51
DrosopoulosS.WindauE.WagnerU.BornJ. (2007). Sleep enforces the temporal order in memory.PLoS One2:e376. 10.1371/journal.pone.0000376
52
DrummondS. P. A.AndersonD. E.StrausL. D.VogelE. K.PerezV. B. (2012). The effects of two types of sleep deprivation on visual working memory capacity and filtering efficiency.PLoS One7:e35653. 10.1371/journal.pone.0035653
53
DrummondS. P. A.BrownG. G.GillinJ. C.StrickerJ. L.WongE. C.BuxtonR. B. (2000). Altered brain response to verbal learning following sleep deprivation.Nature403655–657.
54
DudaM.DomagalikA.Orlowska-FeuerP.Krzysztynska-KuletaO.BeldzikE.SmykM. K.et al (2020). Melanopsin: From a small molecule to brain functions.Neurosci. Biobehav. Rev.113190–203. 10.1016/j.neubiorev.2020.03.012
55
DurmerJ. S.PhD.DingesD. F.PhD. (2005). Neurocognitive consequences of sleep deprivation.Semin. Neurol.25117–129.
56
EichenbaumH. (1999). The hippocampus and mechanisms of declarative memory.Behav. Brain Res.103123–133.
57
EichenbaumH. (2004). Hippocampus: Cognitive processes and neural representations that underlie declarative memory.Neuron44109–120. 10.1016/j.neuron.2004.08.028
58
EllenbogenJ. M.HulbertJ. C.JiangY.StickgoldR. (2009). The sleeping brain’s influence on verbal memory: Boosting resistance to interference.PLoS One4:2–5. 10.1371/journal.pone.0004117
59
EsakiY.KitajimaT.ItoY.KoikeS.NakaoY.TsuchiyaA.et al (2016). Wearing blue light-blocking glasses in the evening advances circadian rhythms in the patients with delayed sleep phase disorder: an open-label trial.Chronobiol. Int.331037–1044. 10.1080/07420528.2016.1194289
60
EschenkoO.RamadanW.MölleM.BornJ.SaraS. J. (2008). Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning.Learn. Mem.15222–228. 10.1101/lm.726008
61
FalloneG.AceboC.ArnedtJ. T.SeiferR.CarskadonM. A. (2001). Effects of acute sleep restriction on behavior, sustained attention, and response inhibition in children.Percept. Mot. Skills93213–229. 10.2466/pms.2001.93.1.213
62
FeldG. B.WeisP. P.BornJ. (2016). The limited capacity of sleep-dependent memory consolidation.Front. Psychol.7:1368. 10.3389/fpsyg.2016.01368
63
FennK. M.GalloD. A.MargoliashD.RoedigerH. L.NusbaumH. C. (2009). Reduced false memory after sleep.Learn. Mem.16509–513. 10.1101/lm.1500808
64
FisherS. P.FosterR. G.PeirsonS. N. (2013). The circadian control of sleep.Handbook Exp. Pharmacol.217157–183.
65
GaisS.AlbouyG.BolyM.Dang-VuT. T.DarsaudA.DesseillesM.et al (2007). Sleep transforms the cerebral trace of declarative memories.Proc. Natl. Acad. Sci. U.S.A.10418778–18783. 10.1073/pnas.0705454104
66
GaisS.LucasB.BornJ. (2006). Sleep after learning aids memory recall.Learn. Mem.13259–262. 10.1101/lm.132106
67
GradisarM.TerrillG.JohnstonA.DouglasP. (2008). Adolescent sleep and working memory performance.Sleep Biol. Rhythms6146–154.
68
GrantL. K.KentB. A.MayerM. D.StickgoldR.LockleyS. W.RahmanS. A. (2021). Daytime exposure to short wavelength-enriched light improves cognitive performance in sleep-restricted college-aged adults.Front. Neurol.12:624217. 10.3389/fneur.2021.624217
69
GriessenbergerH.HoedlmoserK.HeibD. P. J.LechingerJ.KlimeschW.SchabusM. (2012). Consolidation of temporal order in episodic memories.Biol. Psychol.91150–155. 10.1016/j.biopsycho.2012.05.012
70
GujarN.YooS. S.HuP.WalkerM. P. (2010). The unrested resting brain: sleep deprivation alters activity within the default-mode network.J. Cogn. Neurosci221637–1648. 10.1162/jocn.2009.21331
71
GujarN.YooS. S.HuP.WalkerM. P. (2011). Sleep deprivation amplifies reactivity of brain reward networks, biasing the appraisal of positive emotional experiences.J. Neurosci314466–4474. 10.1523/JNEUROSCI.3220-10.2011
72
HabeckC.RakitinB. C.MoellerJ.ScarmeasN.ZarahnE.BrownT.et al (2004). An event-related fMRI study of the neurobehavioral impact of sleep deprivation on performance of a delayed-match-to-sample task.Cogn. Brain Res.18306–321. 10.1016/j.cogbrainres.2003.10.019
73
HankinsM. W.PeirsonS. N.FosterR. G. (2008). Melanopsin: an exciting photopigment.Trends Neurosci.3127–36. 10.1016/j.tins.2007.11.002
74
HarveyA. G.SchmidtD. A.ScarnàA.SemlerC. N.GoodwinG. M. (2005). Sleep-related functioning in euthymic patients with bipolar disorder, patients with insomnia, and subjects without sleep problems.Am. J. Psychiatry16250–57. 10.1176/appi.ajp.162.1.50
75
HeydeI.OsterH. (2019). Differentiating external zeitgeber impact on peripheral circadian clock resetting.Sci. Rep.91–13. 10.1038/s41598-019-56323-z
76
HirshkowitzM.WhitonK.AlbertS. M.AlessiC.BruniO.DonCarlosL. (2015). National sleep foundation’s sleep time duration recommendations: Methodology and results summary.Sleep Health140–43. 10.1016/j.sleh.2014.12.010
77
HornungO. P.RegenF.Danker-HopfeH.SchredlM.HeuserI. (2007). The Relationship Between REM Sleep and Memory Consolidation in Old Age and Effects of Cholinergic Medication.Biol. Psychiatry61750–757. 10.1016/j.biopsych.2006.08.034
78
HouJ.ShenQ.WanX.ZhaoB.WuY.XiaZ. (2019). REM sleep deprivation-induced circadian clock gene abnormalities participate in hippocampal-dependent memory impairment by enhancing inflammation in rats undergoing sevoflurane inhalation.Behav. Brain Res.364167–176. 10.1016/j.bbr.2019.01.038
79
HuangW.RamseyK. M.MarchevaB.BassJ. (2011). Circadian rhythms, sleep, and metabolism.J. Clin. Invest.1212133–2141.
80
IbukaN.InouyeS. T.KawamuraH. (1977). Analysis of sleep-wakefulness rhythms in male rats after suprachiasmatic nucleus lesions and ocular enucleation.Brain Res.12233–47. 10.1016/0006-8993(77)90660-6
81
InostrozaM.BornJ. (2013). Sleep for preserving and transforming episodic memory.Annu. Rev. Neurosci.3679–102. 10.1146/annurev-neuro-062012-170429
82
JacksonM. L.GunzelmannG.WhitneyP.HinsonJ. M.BelenkyG.RabatA.et al (2013). Deconstructing and reconstructing cognitive performance in sleep deprivation.Sleep Med. Rev.17215–225. 10.1016/j.smrv.2012.06.007
83
JacksonM. L.HughesM. E.CroftR. J.HowardM. E.CrewtherD.KennedyG. A.et al (2011). The effect of sleep deprivation on BOLD activity elicited by a divided attention task.Brain Imaging Behav.597–108. 10.1007/s11682-011-9115-6
84
JenningsJ. R.MonkT. H.Van der MolenM. W. (2003). Sleep deprivation influences some but not all processes of supervisory attention.Psychol. Sci.14473–479. 10.1111/1467-9280.02456
85
JiD.WilsonM. A. (2007). Coordinated memory replay in the visual cortex and hippocampus during sleep.Nat. Neurosci.10100–107. 10.1038/nn1825
86
KormanM.RazN.FlashT.KarniA. (2003). Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance.Proc. Natl. Acad. Sci. U.S.A.10012492–12497. 10.1073/pnas.2035019100
87
KrauseA. J.SimonE.Ben ManderB. A.GreerS. M.SaletinJ. M.Goldstein-PiekarskiA. N.et al (2017). The sleep-deprived human brain.Nat. Rev. Neurosci.18404–418. 10.1038/nrn.2017.55
88
KuriyamaK.MishimaK.SuzukiH.AritakeS.UchiyamaM. (2008). Sleep accelerates the improvement in working memory performance.J. Neurosci.2810145–10150. 10.1523/JNEUROSCI.2039-08.2008
89
LackL.BramwellT.WrightH.KempK. (2007). Morning blue light can advance the melatonin rhythm in mild delayed sleep phase syndrome.Sleep Biol. Rhythms578–80.
90
LeeS. H.BakerC. I. (2016). Multi-voxel decoding and the topography of maintained information during visual working memory.Front. Syst. Neurosci10:2. 10.3389/fnsys.2016.00002
91
LibedinskyC.SmithD. V.TengC. S.NamburiP.ChenV. W.HuettelS. A.et al (2011). Sleep deprivation alters valuation signals in the ventromedial prefrontal cortex.Front. Behav. Neurosci5:70. 10.3389/fnbeh.2011.00070
92
LimJ.ChooW. C.CheeM. W. L. (2007). Reproducibility of changes in behaviour and fMRI activation associated with sleep deprivation in a working memory task.Sleep3061–70. 10.1093/sleep/30.1.61
93
LimJ.TanJ. C.ParimalS.DingesD. F.CheeM. W. L. (2010). Sleep deprivation impairs object-selective attention: a view from the ventral visual cortex.PLoS One5:e9087. 10.1371/journal.pone.0009087
94
LoJ. C.GroegerJ. A.ChengG. H.DijkD. J.CheeM. W. L. (2016). Self-reported sleep duration and cognitive performance in older adults: a systematic review and meta-analysis.Sleep Med.1787–98. 10.1016/j.sleep.2015.08.021
95
LuberB.StanfordA. D.BulowP.NguyenT.RakitinB. C.HabeckC.et al (2008). Remediation of sleep-deprivation-induced working memory impairment with fMRI-guided transcranial magnetic stimulation.Cereb. Cortex182077–2085. 10.1093/cercor/bhm231
96
LutzN. D.DiekelmannS.Hinse-SternP.BornJ.RaussK. (2017). Sleep Supports the Slow Abstraction of GIST from Visual Perceptual Memories.Sci. Rep.71–9. 10.1038/srep42950
97
LytheK. E.WilliamsS. C. R.AndersonC.LibriV.MehtaM. A. (2012). Frontal and parietal activity after sleep deprivation is dependent on task difficulty and can be predicted by the fMRI response after normal sleep.Behav. Brain Res.23362–70. 10.1016/j.bbr.2012.04.050
98
MacDonaldK. J.LockhartH. A.StoraceA. C.EmrichS. M.CoteK. A. (2018). A daytime nap enhances visual working memory performance and alters event-related delay activity.Cogn. Affect. Behav. Neurosci.181105–1120. 10.3758/s13415-018-0625-1
99
ManderB. A.ReidK. J.DavuluriV. K.SmallD. M.ParrishT. B.MesulamM. M.et al (2008). Sleep deprivation alters functioning within the neural network underlying the covert orienting of attention.Brain Res.1217148–156. 10.1016/j.brainres.2008.04.030
100
MannsJ. R.EichenbaumH. (2006). Evolution of declarative memory.Hippocampus16795–808. 10.1002/hipo.20205
101
MarkwellE. L.FeiglB.ZeleA. J. (2010). Intrinsically photosensitive melanopsin retinal ganglion cell contributions to the pupillary light reflex and circadian rhythm.Clin. Exp. Optom.93137–149. 10.1111/j.1444-0938.2010.00479.x
102
MascettiL.MutoV.MatarazzoL.ForetA.ZieglerE.AlbouyG.et al (2013). The impact of visual perceptual learning on sleep and local slow-wave initiation.J. Neurosci.333323–3331. 10.1523/JNEUROSCI.0763-12.2013
103
MuQ.NahasZ.JohnsonK. A.YamanakaK.MishoryA.KoolaJ.et al (2005a). Decreased cortical response to verbal working memory following sleep deprivation.Sleep2855–67. 10.1093/sleep/28.1.55
104
MuQ.MishoryA.JohnsonK. A.NahasZ.KozelF. A.YamanakaK.et al (2005b). Decreased brain activation during a working memory task at rested baseline is associated with vulnerability to sleep deprivation.Sleep28433–446. 10.1093/sleep/28.4.433
105
MurrayG.HarveyA. (2010). Circadian rhythms and sleep in bipolar disorder.Bipolar Disord.12459–472.
106
Nathan SprengR.DupreE.SelarkaD.GarciaJ.GojkovicS.MildnerJ.et al (2014). Goal-congruent default network activity facilitates cognitive control.J. Neurosci.3414108–14114. 10.1523/JNEUROSCI.2815-14.2014
107
NinadG.Seung-SchikY.PeterH.MatthewP. W. (2010). The un-rested resting brain: sleep-deprivation alters activity within the default-mode network.Bone221637–1648.
108
NirY.AndrillonT.MarmelshteinA.SuthanaN.CirelliC.TononiG.et al (2017). Selective neuronal lapses precede human cognitive lapses following sleep deprivation Yuval.Nat. Med.231474–1480. 10.1038/nm.4433
109
NotaJ. A.ColesM. E. (2018). Shorter sleep duration and longer sleep onset latency are related to difficulty disengaging attention from negative emotional images in individuals with elevated transdiagnostic repetitive negative thinking.J. Behav. Ther. Exp. Psychiatry58114–122. 10.1016/j.jbtep.2017.10.003
110
NumssenO.BzdokD.HartwigsenG. (2020). Hemispheric specialization within the inferior parietal lobe across cognitive domains.elife251–25.
111
OngJ. L.LoJ. C.GooleyJ. J.CheeM. W. L. (2016). EEG changes across multiple nights of sleep restriction and recovery in adolescents: The need for sleep study.Sleep391233–1240. 10.5665/sleep.5840
112
PallerK. A.VossJ. L. (2004). Memory reactivation and consolidation during sleep.Learn. Mem.11664–670.
113
PandaS.NayakS. K.CampoB.WalkerJ. R.HogeneschJ. B.JeglaT. (2005). Illumination of the melanopsin signaling pathway.Science307600–604. 10.1126/science.1105121
114
PaxtonJ. L.BarchD. M.RacineC. A.BraverT. S. (2008). Cognitive control, goal maintenance, and prefrontal function in healthy aging.Cereb. Cortex181010–1028. 10.1093/cercor/bhm135
115
PayneJ. D.SchacterD. L.PropperR. E.HuangL. W.WamsleyE. J.TuckerM. A.et al (2009). The role of sleep in false memory formation.Neurobiol. Learn. Mem.92327–334. 10.1016/j.nlm.2009.03.007
116
PennartzC. M. A.UylingsH. B. M.BarnesC. A.McNaughtonB. L. (2002). Memory reactivation and consolidation during sleep: From cellular mechanisms to human performance.Prog. Brain Res.138143–166. 10.1016/S0079-6123(02)38076-2
117
PlihalW.BornJ. (1997). Effects of early and late nocturnal sleep on declarative and procedural memory.J. Cogn. Neurosci.9534–547.
118
Porkka-HeiskanenT. (2013). Sleep homeostasis.Curr. Opin. Neurobiol.23799–805.
119
Prehn-KristensenA.GöderR.ChirobejaS.BreßmannI.FerstlR.BavingL. (2009). Sleep in children enhances preferentially emotional declarative but not procedural memories.J. Exp. Child Psychol.104132–139. 10.1016/j.jecp.2009.01.005
120
RamadanW.EschenkoO.SaraS. J. (2009). Hippocampal sharp wave/ripples during sleep for consolidation of associative memory.PLoS One4:e6697. 10.1371/journal.pone.0006697
121
RaschB.BornJ. (2013). About sleep’s role in memory.Physiol. Rev.102681–766.
122
RaschB.BüchelC.GaisS.BornJ. (2007). Odor cues during slow-wave sleep prompt declarative memory consolidation.Science3151426–1429.
123
RatcliffR.van DongenH. P. A. (2009). Sleep deprivation affects multiple distinct cognitive processes.Psychon. Bull. Rev.16742–751. 10.3758/PBR.16.4.742
124
RauchsG.BertranF.Guillery-GirardB.DesgrangesB.KerroucheN.DeniseP.et al (2004). Consolidation of strictly episodic memories mainly requires rapid eye movement sleep.Sleep27395–401. 10.1093/sleep/27.3.395
125
RawashdehO.MarondeE. (2012). The hormonal Zeitgeber melatonin: Role as a circadian modulator in memory processing.Front. Mol. Neurosci.5:27. 10.3389/fnmol.2012.00027
126
RedinbaughM. J.PhillipsJ. M.KambiN. A.MohantaS.AndrykS.DooleyG. L.et al (2020). Thalamus modulates consciousness via layer-specific control of cortex.Neuron10666.e–75.e. 10.1016/j.neuron.2020.01.005
127
RiemersmaR. F.MattheijC. A. M.SwaabD. F.Van SomerenE. J. W. (2004). Melatonin rhythms, melatonin supplementation and sleep in old age.Neur. Biol.41723–1729.
128
RobertsR. E.DuongH. T. (2014). The prospective association between sleep deprivation and depression among adolescents.Sleep37239–244. 10.5665/sleep.3388
129
Rosales-LagardeA.ArmonyJ. L.del Río-PortillaY.Trejo-MartínezD.CondeR.Corsi-CabreraM. (2012). Enhanced emotional reactivity after selective REM sleep deprivation in humans: an fMRI study.Front. Behav. Neurosci.6:25. 10.3389/fnbeh.2012.00025
130
RubyN. F.BrennanT. J.XieX.CaoV.FrankenP.HellerH. C.et al (2002). Role of melanopsin in circadian responses to light.Science2982211–2213. 10.1126/science.1076701
131
SateiaM. J. (2014). International classification of sleep disorders-third edition highlights and modifications.Chest1461387–1394.
132
SchreinerT.RaschB. (2017). The beneficial role of memory reactivation for language learning during sleep: a review.Brain Lang.16794–105. 10.1016/j.bandl.2016.02.005
133
ShenC. Y.XuZ.ZhaoS. L.HuangQ. Y. (2014). Study on the safety of blue light leak of LED. guang pu xue yu guang pu fen xi/spectroscopy spectr.Anal34:180.
134
SlettenT. L.RevellV. L.MiddletonB.LederleK. A.SkeneD. J. (2009). Age-related changes in acute and phase-advancing responses to monochromatic light.J. Biol. Rhythms2473–84. 10.1177/0748730408328973
135
SquireL. R.ZolaS. M. (1996). Structure and function of declarative and nondeclarative memory systems.Proc. Natl. Acad. Sci. U.S.A.9313515–13522. 10.1073/pnas.93.24.13515
136
SteriadeM.LlinasR. R. (1988). The functional states of the thalamus and the associated neuronal interplay.Physiol. Rev.68649–724. 10.1152/physrev.1988.68.3.649
137
SterpenichV.CeravoloL.SchwartzS. (2017). Sleep deprivation disrupts the contribution of the hippocampus to the formation of novel lexical associations.Brain Lang.16761–71. 10.1016/j.bandl.2016.12.007
138
StickgoldR.JamesL.HobsonJ. A. (2000a). Visual discrimination learning requires sleep after training.Nat. Neurosci.31237–1238. 10.1038/81756
139
StickgoldR.WhidbeeD.SchirmerB.PatelV.HobsonJ. A. (2000b). Visual discrimination task improvement: a multi-step process occurring during sleep.J. Cogn. Neurosci.12246–254. 10.1162/089892900562075
140
TempestaD.SocciV.Dello IoioG.De GennaroL.FerraraM. (2017). The effect of sleep deprivation on retrieval of emotional memory: a behavioural study using film stimuli.Exp. Brain Res.2353059–3067. 10.1007/s00221-017-5043-z
141
TsaiJ. W.HannibalJ.HagiwaraG.ColasD.RuppertE.RubyN. F.et al (2009). Melanopsin as a sleep modulator: Circadian gating of the direct effects of light on sleep and altered sleep homeostasis in Opn4-/- mice.PLoS Biol7:e1000125. 10.1371/journal.pbio.1000125
142
TulvingE.MarkowitschH. J. (1998). Episodic and declarative memory: Role of the hippocampus.Hippocampus8198–204. 10.1002/(SICI)1098-1063(1998)8:3<198::AID-HIPO2>3.0.CO;2-G
143
UtevskyA. V.SmithD. V.HuettelS. A. (2014). Precuneus is a functional core of the default-mode network.J. Neurosci.34932–940.
144
van der HelmE.GujarN.NishidaM.WalkerM. P. (2011). Sleep-dependent facilitation of episodic memory details.PLoS One6:e27421. 10.1371/journal.pone.0027421
145
Van Der WerfY. D.AltenaE.SchoonheimM. M.Sanz-ArigitaE. J.VisJ. C.De RijkeW.et al (2009). Sleep benefits subsequent hippocampal functioning.Nat. Neurosci.12122–123. 10.1038/nn.2253
146
VandewalleG.MaquetP.DijkD. J. (2009). Light as a modulator of cognitive brain function.Trends Cogn. Sci.13429–438. 10.1016/j.tics.2009.07.004
147
VersaceF.CavalleroC.De Min TonaG.MozzatoM.StegagnoL. (2006). Effects of sleep reduction on spatial attention.Biol. Psychol.71248–255. 10.1016/j.biopsycho.2005.04.003
148
WagnerA. D.MarilA.BjorkR. A.SchacterD. L. (2001). Prefrontal contributions to executive control: fMRI evidence for functional distinctions within lateral prefrontal cortex.Neuroimage141337–1347. 10.1006/nimg.2001.0936
149
WalkerM. P. (2009). The role of sleep in cognition and emotion.Ann N Y Acad Sci.1156168–197. 10.1111/j.1749-6632.2009.04416.x
150
WalkerM. P.BrakefieldT.MorganA.HobsonJ. A.StickgoldR. (2002). Practice with sleep makes perfect: Sleep-dependent motor skill learning.Neuron35205–211. 10.1016/s0896-6273(02)00746-8
151
WangL.ChenY.YaoY.PanY.SunY. (2016). Sleep deprivation disturbed regional brain activity in healthy subjects: Evidence from a functional magnetic resonance-imaging study.Neuropsychiatr. Dis. Treat.12801–807. 10.2147/NDT.S99644
152
WarmanV. L.DijkD. J.WarmanG. R.ArendtJ.SkeneD. J. (2003). Phase advancing human circadian rhythms with short wavelength light.Neurosci. Lett.34237–40. 10.1016/s0304-3940(03)00223-4
153
WeingartenJ. A.CollopN. A. (2013). Air travel: effects of sleep deprivation and jet lag.Chest1441394–1401. 10.1378/chest.12-2963
154
WrightH. R.LackL. C.KennawayD. J. (2004). Differential effects of light wavelength in phase advancing the melatonin rhythm.J. Pineal Res.36140–144. 10.1046/j.1600-079x.2003.00108.x
155
WulffK.DijkD. J.MiddletonB.FosterR. G.JoyceE. M. (2012). Sleep and circadian rhythm disruption in schizophrenia.Br. J. Psychiatry200308–316.
156
XieW.BerryA.LustigC.DeldinP.ZhangW. (2019). Poor sleep quality and compromised visual working memory capacity.J. Int. Neuropsychol. Soc.25583–594. 10.1017/S1355617719000183
157
YooS. S.HuP. T.GujarN.JoleszF. A.WalkerM. P. (2007). A deficit in the ability to form new human memories without sleep.Nat. Neurosci.10385–392. 10.1038/nn1851
158
YuJ.RawtaerI.FamJ.JiangM. J.FengL.KuaE. H.et al (2016). Sleep correlates of depression and anxiety in an elderly asian population.Psychogeriatrics16191–195. 10.1111/psyg.12138
159
ZhaoR.ZhangX.FeiN.ZhuY.SunJ.LiuP.et al (2019). Decreased cortical and subcortical response to inhibition control after sleep deprivation.Brain Imaging Behav.13638–650. 10.1007/s11682-018-9868-2
Summary
Keywords
sleep deprivation, circadian rhythm, long-term memory, cognitive control, light
Citation
Kim T, Kim S, Kang J, Kwon M and Lee S-H (2022) The Common Effects of Sleep Deprivation on Human Long-Term Memory and Cognitive Control Processes. Front. Neurosci. 16:883848. doi: 10.3389/fnins.2022.883848
Received
25 February 2022
Accepted
11 May 2022
Published
02 June 2022
Volume
16 - 2022
Edited by
Luis de Lecea, Stanford University, United States
Reviewed by
Ciro della Monica, University of Surrey, United Kingdom; Vincenzo Natale, University of Bologna, Italy
Updates
Copyright
© 2022 Kim, Kim, Kang, Kwon and Lee.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Sue-Hyun Lee, suelee@kaist.ac.kr
†These authors have contributed equally to this work
This article was submitted to Sleep and Circadian Rhythms, a section of the journal Frontiers in Neuroscience
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.