Person: Stickgold, Robert
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Stickgold
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Stickgold, Robert
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Publication Recurrence of task-related electroencephalographic activity during post-training quiet rest and sleep(Nature Publishing Group UK, 2018) Murphy, Michael; Stickgold, Robert; Parr, Mittie Elaine; Callahan, Cameron; Wamsley, Erin J.Offline reactivation of task-related neural activity has been demonstrated in animals but is difficult to directly observe in humans. We sought to identify potential electroencephalographic (EEG) markers of offline memory processing in human subjects by identifying a set of characteristic EEG topographies (“microstates”) that occurred as subjects learned to navigate a virtual maze. We hypothesized that these task-related microstates would appear during post-task periods of rest and sleep. In agreement with this hypothesis, we found that one task-related microstate was increased in post-training rest and sleep compared to baseline rest, selectively for subjects who actively learned the maze, and not in subjects performing a non-learning control task. Source modeling showed that this microstate was produced by activity in temporal and parietal networks, which are known to be involved in spatial navigation. For subjects who napped after training, the increase in this task-related microstate predicted the magnitude of subsequent change in performance. Our findings demonstrate that task-related EEG patterns re-emerge during post-training rest and sleep.Publication Individual Differences in Frequency and Topography of Slow and Fast Sleep Spindles(Frontiers Media S.A., 2017) Cox, Roy; Schapiro, Anna; Manoach, Dara; Stickgold, RobertSleep spindles are transient oscillatory waveforms that occur during non-rapid eye movement (NREM) sleep across widespread cortical areas. In humans, spindles can be classified as either slow or fast, but large individual differences in spindle frequency as well as methodological difficulties have hindered progress towards understanding their function. Using two nights of high-density electroencephalography recordings from 28 healthy individuals, we first characterize the individual variability of NREM spectra and demonstrate the difficulty of determining subject-specific spindle frequencies. We then introduce a novel spatial filtering approach that can reliably separate subject-specific spindle activity into slow and fast components that are stable across nights and across N2 and N3 sleep. We then proceed to provide detailed analyses of the topographical expression of individualized slow and fast spindle activity. Group-level analyses conform to known spatial properties of spindles, but also uncover novel differences between sleep stages and spindle classes. Moreover, subject-specific examinations reveal that individual topographies show considerable variability that is stable across nights. Finally, we demonstrate that topographical maps depend nontrivially on the spindle metric employed. In sum, our findings indicate that group-level approaches mask substantial individual variability of spindle dynamics, in both the spectral and spatial domains. We suggest that leveraging, rather than ignoring, such differences may prove useful to further our understanding of the physiology and functional role of sleep spindles.Publication Untreated Sleep-Disordered Breathing: Links to Aging-Related Decline in Sleep-Dependent Memory Consolidation(Public Library of Science, 2014) Djonlagic, Ina; Guo, Mengshuang; Matteis, Paul; Carusona, Andrea; Stickgold, Robert; Malhotra, AtulBackground: Increasing age is associated with a decline in cognition and motor skills, while at the same time exacerbating one's risk of developing obstructive sleep apnea (OSA). OSA-related cognitive deficits are highly prevalent and can affect various memory systems including overnight memory consolidation on a motor sequence task. Thus, the aim of our study was to examine the effect of aging on sleep-dependent motor memory consolidation in patients with and without OSA. Methods: We studied 44 patients (19–68 years) who had been referred by a physician for a baseline polysomnography (PSG) evaluation. Based on their PSG, patients were assigned either to the OSA group (AHI>5/h), or control (Non-OSA) group (AHI<5/h). All subjects performed the Psychomotor Vigilance Task (PVT) and the Motor Sequence Learning Task (MST) in the evening and again in the morning after their PSG. Results: Despite similar learning in the evening, OSA subjects showed significantly less overnight improvement on the MST, both for immediate (OSA −2.7%±2.8% vs. controls 12.2%±3.5%; p = 0.002) and plateau improvement (OSA 4.9%±2.3% vs. controls 21.1%±4.0%; p = 0.001). Within the OSA group, there was a significant negative correlation between overnight MST improvement and age (r2 = 0.3; p = 0.01), an effect that was not observed in the Non-OSA group (r2 = 0.08; p = 0.23) Conclusions: Consistent with previous research, healthy sleepers demonstrated a higher degree of sleep-dependent overnight improvement on the MST, an effect not mitigated by increasing age. However, the presence of untreated obstructive sleep apnea is associated with an aging-related cognitive deficit, otherwise not present in individuals without OSA. As other research has linked the presence of OSA to a higher likelihood of developing dementia, future studies are necessary to examine if the inhibition of memory consolidation is tied to the onset of neurodegenerative disease.Publication Sleep spindle deficits in antipsychotic-naïve early course schizophrenia and in non-psychotic first-degree relatives(Frontiers Media S.A., 2014) Manoach, Dara; Demanuele, Charmaine; Wamsley, Erin J.; Vangel, Mark; Montrose, Debra M.; Miewald, Jean; Kupfer, David; Buysse, Daniel; Stickgold, Robert; Keshavan, MatcheriIntroduction: Chronic medicated patients with schizophrenia have marked reductions in sleep spindle activity and a correlated deficit in sleep-dependent memory consolidation. Using archival data, we investigated whether antipsychotic-naïve early course patients with schizophrenia and young non-psychotic first-degree relatives of patients with schizophrenia also show reduced sleep spindle activity and whether spindle activity correlates with cognitive function and symptoms. Method: Sleep spindles during Stage 2 sleep were compared in antipsychotic-naïve adults newly diagnosed with psychosis, young non-psychotic first-degree relatives of schizophrenia patients and two samples of healthy controls matched to the patients and relatives. The relations of spindle parameters with cognitive measures and symptom ratings were examined. Results: Early course schizophrenia patients showed significantly reduced spindle activity relative to healthy controls and to early course patients with other psychotic disorders. Relatives of schizophrenia patients also showed reduced spindle activity compared with controls. Reduced spindle activity correlated with measures of executive function in early course patients, positive symptoms in schizophrenia and IQ estimates across groups. Conclusions: Like chronic medicated schizophrenia patients, antipsychotic-naïve early course schizophrenia patients and young non-psychotic relatives of individuals with schizophrenia have reduced sleep spindle activity. These findings indicate that the spindle deficit is not an antipsychotic side-effect or a general feature of psychosis. Instead, the spindle deficit may predate the onset of schizophrenia, persist throughout its course and be an endophenotype that contributes to cognitive dysfunction.Publication Sleep spindle and slow wave frequency reflect motor skill performance in primary school-age children(Frontiers Media S.A., 2014) Astill, Rebecca G.; Piantoni, Giovanni; Raymann, Roy J. E. M.; Vis, Jose C.; Coppens, Joris E.; Walker, Matthew P.; Stickgold, Robert; Van Der Werf, Ysbrand D.; Van Someren, Eus J. W.Background and Aim: The role of sleep in the enhancement of motor skills has been studied extensively in adults. We aimed to determine involvement of sleep and characteristics of spindles and slow waves in a motor skill in children. Hypothesis: We hypothesized sleep-dependence of skill enhancement and an association of interindividual differences in skill and sleep characteristics. Methods:: 30 children (19 females, 10.7 ± 0.8 years of age; mean ± SD) performed finger sequence tapping tasks in a repeated-measures design spanning 4 days including 1 polysomnography (PSG) night. Initial and delayed performance were assessed over 12 h of wake; 12 h with sleep; and 24 h with wake and sleep. For the 12 h with sleep, children were assigned to one of three conditions: modulation of slow waves and spindles was attempted using acoustic perturbation, and compared to yoked and no-sound control conditions. Analyses: Mixed effect regression models evaluated the association of sleep, its macrostructure and spindles and slow wave parameters with initial and delayed speed and accuracy. Results and Conclusions: Children enhance their accuracy only over an interval with sleep. Unlike previously reported in adults, children enhance their speed independent of sleep, a capacity that may to be lost in adulthood. Individual differences in the dominant frequency of spindles and slow waves were predictive for performance: children performed better if they had less slow spindles, more fast spindles and faster slow waves. On the other hand, overnight enhancement of accuracy was most pronounced in children with more slow spindles and slower slow waves, i.e., the ones with an initial lower performance. Associations of spindle and slow wave characteristics with initial performance may confound interpretation of their involvement in overnight enhancement. Slower frequencies of characteristic sleep events may mark slower learning and immaturity of networks involved in motor skills.Publication Experience Playing a Musical Instrument and Overnight Sleep Enhance Performance on a Sequential Typing Task(Public Library of Science, 2016) Tucker, Matthew A.; Nguyen, Nam; Stickgold, RobertThe smooth, coordinated fine motor movements required to play a musical instrument are not only highly valued in our society; they also predict academic success in areas that generalize beyond the motor domain, including reading and math readiness, and verbal abilities. Interestingly, motor skills that overlap with those required to play a musical instrument (e.g., sequential finger tapping) markedly improve (get faster) over a night of sleep, but not after a day spent awake. Here we studied whether individuals who play musical instruments that require fine finger motor skill are better able to learn and consolidate a simple motor skill task compared to those who do not play an instrument, and whether sleep-specific motor skill benefits interact with those imparted by musical experience. We used the motor sequence task (MST), which taps into a core skill learned and used by musicians, namely, the repetition of learned sequences of key presses. Not surprisingly, we found that musicians were faster than non-musicians throughout the learning session, typing more correct sequences per 30-sec trial. In the 12hrs that followed learning we found that sleep and musical experience both led to greater improvement in performance. Surprisingly, musicians retested after a day of wake performed slightly better than non-musicians who had slept between training and retest, suggesting that musicians have the capacity to consolidate a motor skill across waking hours, while non-musicians appear to lack this capacity. These findings suggest that the musically trained brain is optimized for motor skill consolidation across both wake and sleep, and that sleep may simply promote a more effective use of this machinery. In sum, there may be something special about musicians, perhaps a neurophysiological advantage, that leads to both the expected—greater motor speed at learning—and the surprising—greater motor skill improvement over time.Publication Memory for Semantically Related and Unrelated Declarative Information: The Benefit of Sleep, the Cost of Wake(Public Library of Science, 2012) Payne, Jessica D.; Tucker, Matthew; Ellenbogen, Jeffrey Michael; Wamsley, Erin; Walker, Matthew P.; Schacter, Daniel; Stickgold, RobertNumerous studies have examined sleep's influence on a range of hippocampus-dependent declarative memory tasks, from text learning to spatial navigation. In this study, we examined the impact of sleep, wake, and time-of-day influences on the processing of declarative information with strong semantic links (semantically related word pairs) and information requiring the formation of novel associations (unrelated word pairs). Participants encoded a set of related or unrelated word pairs at either 9am or 9pm, and were then tested after an interval of 30 min, 12 hr, or 24 hr. The time of day at which subjects were trained had no effect on training performance or initial memory of either word pair type. At 12 hr retest, memory overall was superior following a night of sleep compared to a day of wakefulness. However, this performance difference was a result of a pronounced deterioration in memory for unrelated word pairs across wake; there was no sleep-wake difference for related word pairs. At 24 hr retest, with all subjects having received both a full night of sleep and a full day of wakefulness, we found that memory was superior when sleep occurred shortly after learning rather than following a full day of wakefulness. Lastly, we present evidence that the rate of deterioration across wakefulness was significantly diminished when a night of sleep preceded the wake period compared to when no sleep preceded wake, suggesting that sleep served to stabilize the memories against the deleterious effects of subsequent wakefulness. Overall, our results demonstrate that 1) the impact of 12 hr of waking interference on memory retention is strongly determined by word-pair type, 2) sleep is most beneficial to memory 24 hr later if it occurs shortly after learning, and 3) sleep does in fact stabilize declarative memories, diminishing the negative impact of subsequent wakefulness.Publication Increased Sleep Fragmentation Leads to Impaired Off-Line Consolidation of Motor Memories in Humans(Public Library of Science, 2012) Djonlagic, Ina; Saboisky, Julian; Carusona, Andrea; Stickgold, Robert; Malhotra, AtulA growing literature supports a role for sleep after training in long-term memory consolidation and enhancement. Consequently, interrupted sleep should result in cognitive deficits. Recent evidence from an animal study indeed showed that optimal memory consolidation during sleep requires a certain amount of uninterrupted sleep. Sleep continuity is disrupted in various medical disorders. We compared performance on a motor sequence learning task (MST) in relatively young subjects with obstructive sleep apnea (n = 16; apnea-hypopnea index \(17.1 \pm 2.6 / h \) [SEM]) to a carefully matched control group (n = 15, apnea-hypopnea index \(3.7 \pm 0.4 / h\), p<0.001. Apart from AHI, oxygen nadir and arousal index, there were no significant differences between groups in total sleep time, sleep efficiency and sleep architecture as well as subjective measures of sleepiness based on standard questionnaires. In addition performance on the psychomotor vigilance task (reaction time and lapses), which is highly sensitive to sleep deprivation showed no differences as well as initial learning performance during the training phase. However there was a significant difference in the primary outcome of immediate overnight improvement on the MST between the two groups (controls = \(14.7 \pm 4 \% \), patients = \(1.1 \pm 3.6 \% \); \(P = 0.023\) ) as well as plateau performance (controls = \(24.0 \pm 5.3 \% \), patients = \(10.1 \pm 2.0 \% \); \(P = 0.017\) ) and this difference was predicted by the arousal index (p = 0.02) rather than oxygen saturation (nadir and time below 90% saturation. Taken together, this outcome provides evidence that there is a clear minimum requirement of sleep continuity in humans to ensure optimal sleep dependent memory processes. It also provides important new information about the cognitive impact of obstructive sleep apnea and challenges its current definitions.Publication The Sleeping Brain's Influence on Verbal Memory: Boosting Resistance to Interference(Public Library of Science, 2009) Ellenbogen, Jeffrey Michael; Hulbert, Justin C.; Jiang, Ying; Stickgold, RobertMemories evolve. After learning something new, the brain initiates a complex set of post-learning processing that facilitates recall (i.e., consolidation). Evidence points to sleep as one of the determinants of that change. But whenever a behavioral study of episodic memory shows a benefit of sleep, critics assert that sleep only leads to a temporary shelter from the damaging effects of interference that would otherwise accrue during wakefulness. To evaluate the potentially active role of sleep for verbal memory, we compared memory recall after sleep, with and without interference before testing. We demonstrated that recall performance for verbal memory was greater after sleep than after wakefulness. And when using interference testing, that difference was even more pronounced. By introducing interference after sleep, this study confirms an experimental paradigm that demonstrates the active role of sleep in consolidating memory, and unmasks the large magnitude of that benefit.Publication Impaired memory consolidation in children with obstructive sleep disordered breathing(Public Library of Science, 2017) Maski, Kiran; Steinhart, Erin; Holbrook, Hannah; Katz, Eliot S.; Kapur, Kush; Stickgold, RobertMemory consolidation is stabilized and even enhanced by sleep (and particularly by 12–15 Hz sleep spindles in NREM stage 2 sleep) in healthy children but it is unclear what happens to these processes when sleep is disturbed by obstructive sleep disordered breathing. This cross-sectional study investigates differences in declarative memory consolidation among children with primary snoring (PS) and obstructive sleep apnea (OSA) compared to controls. We further investigate whether memory consolidation group differences are associated with NREM stage 2 (N2) sigma (12–15 Hz) or NREM slow oscillation (0.5–1 Hz) spectral power bands. In this study, we trained and tested participants on a spatial declarative memory task with cued recall. Retest occurred after a period of daytime wake (Wake) or a night of sleep (Sleep) with in-lab polysomnography. 36 participants ages 5–9 years completed the protocol: 14 with OSA as defined by respiratory disturbance index (RDI) > 1/hour, 12 with primary snoring (PS) and 10 controls. OSA participants had poorer overall memory consolidation than controls across Wake and Sleep conditions [OSA: mean = -18.7% (5.8), controls: mean = 1.9% (7.2), t = -2.20, P = 0.04]. In contrast, PS participants and controls had comparable memory consolidation across conditions (t = 0.41; P = 0.38). We did not detect a main effect for condition (Sleep, Wake) or group x condition interaction on memory consolidation. OSA participants had lower N2 sigma power than PS (P = 0.03) and controls (P = 0.004) and N2 sigma power inversely correlated with percentage of time snoring on the study night (r = -0.33, P<0.05). Across all participants, N2 sigma power modestly correlated with memory consolidation in both Sleep (r = 0.37, P = 0.03) and Wake conditions (r = 0.44, P = 0.009). Further observed variable path analysis showed that N2 sigma power mediated the relationship between group and mean memory consolidation across Sleep and Wake states [Bindirect = 6.76(3.5), z = 2.03, P = 0.04]. NREM slow oscillation power did not correlate with memory consolidation. All results retained significance after controlling for age and BMI. In sum, participants with mild OSA had impaired memory consolidation and results were mediated by N2 sigma power. These results suggest that N2 sigma power could serve as biomarker of risk for cognitive dysfunction in children with sleep disordered breathing.