Sleep and memory consolidation: motor performance and proactive interference effects in sequence learning.

That post-training sleep supports the consolidation of sequential motor skills remains debated. Performance improvement and sensitivity to proactive interference are both putative measures of long-term memory consolidation. We tested sleep-dependent memory consolidation for visuo-motor sequence learning using a proactive interference paradigm. Thirty-three young adults were trained on sequence A on Day 1, then had Regular Sleep (RS) or were Sleep Deprived (SD) on the night after learning. After two recovery nights, they were tested on the same sequence A, then had to learn a novel, potentially competing sequence B. We hypothesized that proactive interference effects on sequence B due to the prior learning of sequence A would be higher in the RS condition, considering that proactive interference is an indirect marker of the robustness of sequence A, which should be better consolidated over post-training sleep. Results highlighted sleep-dependent improvement for sequence A, with faster RTs overnight for RS participants only. Moreover, the beneficial impact of sleep was specific to the consolidation of motor but not sequential skills. Proactive interference effects on learning a new material at Day 4 were similar between RS and SD participants. These results suggest that post-training sleep contributes to optimizing motor but not sequential components of performance in visuo-motor sequence learning.

Interocular transfer of perceptual skills after sleep.

Several studies suggest that sleep improves perceptual skills in the visual texture discrimination task (TDT). Here we report that besides consolidation, sleep also generalizes the learned perceptual abilities to the untrained eye. Healthy volunteers (n = 32) were trained on the TDT, in which they had to discriminate between horizontal and vertical target textures briefly presented in the periphery of the visual field (left upper quadrant). After a 10-hr interval filled with either sleep or wakefulness, they were retested first on the trained eye in the trained quadrant and then on the untrained eye and quadrant. In line with prior findings, visual discrimination was globally higher after sleep than after wakefulness, as compared to performance levels at the end of training. Furthermore, discrimination performance was significantly improved only in the sleep condition for the untrained eye in the same quadrant, but also showed a trend to generalize to the untrained eye and untrained quadrant. Our results suggest that sleep-dependent perceptual skills continue developing at a later visual-process stage than the V1 area, where learning is not monocular anymore.

Sleep-dependent neurophysiological processes in implicit sequence learning.

Behavioral studies have cast doubts about the role that posttraining sleep may play in the consolidation of implicit sequence learning. Here, we used event-related fMRI to test the hypothesis that sleep-dependent functional reorganization would take place in the underlying neural circuits even in the possible absence of obvious behavioral changes. Twenty-four healthy human adults were scanned at Day 1 and then at Day 4 during an implicit probabilistic serial RT task. They either slept normally (RS) or were sleep-deprived (SD) on the first posttraining night. Unknown to them, the sequential structure of the material was based on a probabilistic finite-state grammar, with 15% chance on each trial of replacing the rules-based grammatical (G) stimulus with a nongrammatical (NG) one. Results indicated a gradual differentiation across sessions between RTs (faster RTs for G than NG), together with NG-related BOLD responses reflecting sequence learning. Similar behavioral patterns were observed in RS and SD participants at Day 4, indicating time- but not sleep-dependent consolidation of performance. Notwithstanding, we observed at Day 4 in the RS group a diminished differentiation between G- and NG-related neurophysiological responses in a set of cortical and subcortical areas previously identified as being part of the network involved in implicit sequence learning and its offline processing during sleep, indicating a sleep-dependent processing of both regular and deviant stimuli. Our results suggest the sleep-dependent development of distinct neurophysiological processes subtending consolidation of implicit motor sequence learning, even in the absence of overt behavioral differences.

Lateralized implicit sequence learning in uni- and bi-manual conditions.

It has been proposed that the right hemisphere (RH) is better suited to acquire novel material whereas the left hemisphere (LH) is more able to process well-routinized information. Here, we ask whether this potential dissociation also manifests itself in an implicit learning task. Using a lateralized version of the serial reaction time task (SRT), we tested whether participants trained in a divided visual field condition primarily stimulating the RH would learn the implicit regularities embedded in sequential material faster than participants in a condition favoring LH processing. In the first study, half of participants were presented sequences in the left (vs. right) visual field, and had to respond using their ipsilateral hand (unimanual condition), hence making visuo-motor processing possible within the same hemisphere. Results showed successful implicit sequence learning, as indicated by increased reaction time for a transfer sequence in both hemispheric conditions and lack of conscious knowledge in a generation task. There was, however, no evidence of interhemispheric differences. In the second study, we hypothesized that a bimanual response version of the lateralized SRT, which requires interhemispheric communication and increases computational and cognitive processing loads, would favor RH-dependent visuospatial/attentional processes. In this bimanual condition, our results revealed a much higher transfer effect in the RH than in the LH condition, suggesting higher RH sensitivity to the processing of novel sequential material. This LH/RH difference was interpreted within the framework of the Novelty-Routinization model [Goldberg, E., & Costa, L. D. (1981). Hemisphere differences in the acquisition and use of descriptive systems. Brain and Language, 14(1), 144-173] and interhemispheric interactions in attentional processing [Banich, M. T. (1998). The missing link: the role of interhemispheric interaction in attentional processing. Brain and Cognition, 36(2), 128-157].

Age-related changes in visual pseudoneglect.

Pseudoneglect is a slight but consistent leftward attentional bias commonly observed in healthy young populations, purportedly explained by right hemispheric dominance. It has been suggested that normal aging might be associated with a decline of the right hemisphere. According to this hypothesis, a few studies have shown that elderly tend to exhibit a rightward attentional bias in line bisection. In the present study, we tested this hypothesis in young and older participants using a perceptual landmark task. Results yield evidence for an age-related shift, from a strong attentional leftward bias in young adults toward a suppressed or even a reversed bias in the elderly. Right hemisphere impairment coupled to a left hemispheric compensation might explain the perceptual shift observed in older adults. However, a decline in corpus callosum function cannot be excluded. Alternatively, these results may be in agreement with the hypothesis of an age-related specific inhibition of return dysfunction, an overt attentional orienting mechanism, and/or a decrease of dopamine.

Reversible Verbal Memory Integration Deficits in Obstructive Sleep Apnoea.

When presented with novel but semantically related elements after learning verbal material, healthy participants tend to endorse these items as previously learned. This reflects the normal integration and association of novel verbal information into long-term memory. How obstructive sleep apnoea (OSA) negatively impacts verbal memory performance, and whether deficits are reversible following positive airway pressure (PAP) treatment, remain elusive. We investigated immediate and delayed OSA- and PAP treatment-related effects on verbal memory integration, using a false memory paradigm. Twenty-three patients with OSA learned lists of words semantically related to target non-presented words (1) at baseline after a polysomnography diagnosis night, (2) after a consecutive polysomnography night under PAP titration, and (3) after three months of compliant PAP treatment. At each session, participants learned 10 different lists of words, each list comprising 15 semantically related items. They had then to recognize 15 minutes later (after an intermediate vigilance task) previously learned words within a list including studied words (learned), unstudied but semantically related items (lures), and non-related unstudied items (controls). Sleep quality and fatigue questionnaires, and psychomotor vigilance tests (PVT) were administered at each session. PAP treatment led to OSA remission and improvement in objective and subjective sleep quality. Crucially, recognition of learned and lure words increased after the first night under treatment and remained stable three months later, suggesting successful memory integration and restoration of semantic processes. No treatment-related outcome was found on PVT performance. OSA exerts a detrimental but PAP-reversible effect on verbal learning and semantic memory integration mechanisms underlying the acquisition of novel memory representations.

Cerebral asymmetries in sleep-dependent processes of memory consolidation.

Preference for previously seen, unfamiliar objects reflects a memory bias on affective judgment, known as the "mere exposure effect" (MEE). Here, we investigated the effect of time, post-exposure sleep, and the brain hemisphere solicited on preference generalization toward objects viewed in different perspectives. When presented in the right visual field (RVF), which promotes preferential processing in the left hemisphere, same and mirrored exemplars were preferred immediately after exposure. MEE generalized to much dissimilar views after three nights of sleep. Conversely, object presentation in the left visual field (LVF), promoting right hemisphere processing, elicited a MEE for same views immediately after exposure, then for mirror views after sleep. Most importantly, sleep deprivation during the first post-exposure night, although followed by two recovery nights, extinguished MEE for all views in the LVF but not in the RVF. Besides demonstrating that post-exposure time and sleep facilitate the generalization process by which we integrate various representations of an object, our results suggest that mostly in the right hemisphere, sleep may be mandatory to consolidate the memory bias underlying affective preference. These interhemispheric differences tentatively call for a reappraisal of the role of cerebral asymmetries in wake- and sleep-dependent processes of memory consolidation.

Spontaneous eyeblinks are sensitive to sequential learning.

Although sequential learning and spontaneous eyeblink rate (EBR) have both been shown to be tightly related to cerebral dopaminergic activity, they have never been investigated at the same time. In the present study, EBR, taken as an indirect marker of dopaminergic activity, was investigated in two resting state conditions, both before and after visuomotor sequence learning in a serial reaction time task (SRT) and during task practice. Participants' abilities to produce and manipulate their knowledge about the sequential material were probed in a generation task. We hypothesized that the time course of spontaneous EBR might follow the progressive decrease of RTs during the SRT session. Additionally, we manipulated the structure of the transfer blocks as well as their respective order, assuming that (1) fully random trials might generate a larger psychophysiological response than an unlearned but structured material, and (2) a second (final) block of transfer might give rise to larger effects given that the sequential material was better consolidated after further practice. Finally, we tentatively hypothesized that, in addition to their online version, spontaneous EBR recorded during the pre- and post-learning resting sessions might be predictive of (1) the SRT learning curve, (2) the magnitude of the transfer effects, and (3) performance in the generation task. Results showed successful sequence learning with decreased accuracy and increased reaction times (RTs) in transfer blocks featuring a different material (random trials or a structured, novel sequence). In line with our hypothesis that EBR reflects dopaminergic activity associated with sequential learning, we observed increased EBR in random trials as well as when the second transfer block occurred at the end of the learning session. There was a positive relationship between the learning curve (RTs) and the slope of EBR during the SRT session. Additionally, inter-individual differences in resting and real-time EBR predicted the magnitude of accuracy and RTs transfer effects, respectively, but they were not related to participants' performances during the generation task. Notwithstanding, our results suggest that the degree of explicit sequential knowledge modulates the association between the magnitude of the transfer effect in EBR and SRT performance. Overall, the present study provides evidence that EBR may represent a valid indirect psychophysiological correlate of dopaminergic activity coupled to sequential learning.

Sleep Deprivation Triggers Cognitive Control Impairments in Task-Goal Switching.

STUDY OBJECTIVES: This study investigates the impact of sleep deprivation (SD) on task-goal switching, a key component of cognitive flexibility. METHODS: Task-goal switching performance was tested after one night of regular sleep (n = 17 participants) or of total SD (n = 18). To understand the relationships between task-switching performance and other cognitive processes following SD, participants were tested for other key attentional (alertness and vigilance) and executive (inhibition and working memory) functions. Spontaneous eye blink rate (EBR) was also measured as an indirect marker of striatal dopaminergic function. RESULTS: SD negatively affects task-goal switching as well as attentional and inhibition measures, but not working memory. Changes in task-goal switching performance were not significantly correlated with changes in objective and subjective markers of fatigue and sleepiness, response inhibition, or spontaneous EBR. CONCLUSIONS: Altogether, our results show differentiated effects of SD on key executive functions such as working memory, inhibition, and task-goal switching.

Lateralized rhythmic acoustic stimulation during daytime NREM sleep enhances slow waves.

Slow wave sleep (SWS) is characterized by the predominance of delta waves and slow oscillations, reflecting the synchronized activity of large cortical neuronal populations. Amongst other functions, SWS plays a crucial role in the restorative capacity of sleep. Rhythmic acoustic stimulation (RAS) during SWS has been shown a cost-effective method to enhance slow wave activity. Slow wave activity can be expressed in a region-specific manner as a function of previous waking activity. However, it is unclear whether slow waves can be enhanced in a region-specific manner using RAS. We investigated the effects of unilaterally presented rhythmic acoustic sound patterns on sleep electroencephalographic (EEG) oscillations. Thirty-five participants received during SWS 12-second long rhythmic bursts of pink noise (at a rate of 1 Hz) that alternated with non-stimulated, silent periods, unilaterally delivered into one of the ears of the participants. As expected, RAS enhanced delta power, especially in its low-frequency components between 0.75 and 2.25 Hz. However, increased slow oscillatory activity was apparent in both hemispheres regardless of the side of the stimulation. The most robust increases in slow oscillatory activity appeared during the first 3-4 seconds of the stimulation period. Furthermore, a short-lasting increase in theta and sigma power was evidenced immediately after the first pulse of the stimulation sequences. Our findings indicate that lateralized RAS has a strong potential to globally enhance slow waves during daytime naps. The lack of localized effects suggests that slow waves are triggered by the ascending reticular system and not directly by specific auditory pathways.

Afternoon nap and bright light exposure improve cognitive flexibility post lunch.

Beneficial effects of napping or bright light exposure on cognitive performance have been reported in participants exposed to sleep loss. Nonetheless, few studies investigated the effect of these potential countermeasures against the temporary drop in performance observed in mid-afternoon, and even less so on cognitive flexibility, a crucial component of executive functions. This study investigated the impact of either an afternoon nap or bright light exposure on post-prandial alterations in task switching performance in well-rested participants. Twenty-five healthy adults participated in two randomized experimental conditions, either wake versus nap (n=15), or bright light versus placebo (n=10). Participants were tested on a switching task three times (morning, post-lunch and late afternoon sessions). The interventions occurred prior to the post-lunch session. In the nap/wake condition, participants either stayed awake watching a 30-minute documentary or had the opportunity to take a nap for 30 minutes. In the bright light/placebo condition, participants watched a documentary under either bright blue light or dim orange light (placebo) for 30 minutes. The switch cost estimates cognitive flexibility and measures task-switching efficiency. Increased switch cost scores indicate higher difficulties to switch between tasks. In both control conditions (wake or placebo), accuracy switch-cost score increased post lunch. Both interventions (nap or bright light) elicited a decrease in accuracy switch-cost score post lunch, which was associated with diminished fatigue and decreased variability in vigilance. Additionally, there was a trend for a post-lunch benefit of bright light with a decreased latency switch-cost score. In the nap group, improvements in accuracy switch-cost score were associated with more NREM sleep stage N1. Thus, exposure to bright light during the post-lunch dip, a countermeasure easily applicable in daily life, results in similar beneficial effects as a short nap on performance in the cognitive flexibility domain with possible additional benefits on latency switch-cost scores.

Implicit learning is better at subjectively defined non-optimal time of day.

Individual preferences in morningness-eveningness rhythms modulate temporal fluctuations of cognitive performance over a normal day. Besides enhanced cognitive performance at individual's peak time as derived from morningness-eveningness questionnaires, a few studies have shown increased implicit memory abilities at a non-optimal (NOP) time of day. Various subjective factors might also determine the clock time for high or low cognitive efficiency. Using an artificial grammar learning (AGL) task, we show enhanced implicit learning of high-order information at NOP [vs optimal (OP)] time of day as subjectively defined by participants, irrespective of morningness-eveningness scores. Our results suggest that subjectively defined efficiency periods are a modulating factor in the testing of cognitive functions.

Lateralized processing of false memories and pseudoneglect in aging.

Aging is associated with higher propensity to false memories and decreased retrieval of previously studied items. When young adults (YA) perform on a lateralized version of the Deese-Roediger-McDermott (DRM) paradigm, the right cerebral hemisphere (RH) is more sensitive than the left (LH) to false memories, suggesting hemispheric imbalance in the cerebral mechanisms supporting semantic and episodic memory processes. Since cerebral asymmetries tend to be reduced with age, we surmised that behavioral asymmetries in the generation of false memories would be diminished with aging. To probe this hypothesis, a lateralized version of the DRM paradigm was administered to healthy older adults (OA) and YA. During the encoding phase, lists of semantically associated words were memorized. During the retrieval session, targets (previously seen words), lures (LU) (never seen strongly semantically related words) and distracters (never seen, unrelated words) were briefly displayed either in the left or right visual fields, thus primarily stimulating the RH or LH, respectively. Participants had to decide whether the word was previously studied (Old/New), but also whether they had a strong episodic recollection (Remember) or a mere feeling of familiarity (Know) about Old words. In line with our predictions, false memories were globally higher in OA than YA, and vivid false recollections (i.e., Remember responses) were higher when LU were presented in the RH in YA, but not in OA. Additionally, we found significant correlations between YA participants' Familiarity scores and leftward attentional bias as previously evidenced using a visuospatial landmark task (Schmitz and Peigneux, 2011), an effect not present in OA. This result is in line with the hypothesis of an interplay between attentional resources allocated to visuospatial and memory processes, suggesting a memory pseudoneglect phenomenon that would be altered with aging.

Sleep unbinds memories from their emotional context.

Consistent evidence nowadays indicates that sleep protects declarative memory from lexical interference. However, little is known about its effect against emotional interference. In a within-subject counterbalanced design, participants learned a list of word pairs after a mood induction procedure (MIP), then slept or stayed awake during the post-learning night. After two recovery nights, half of the list was recalled after a similar mood induction than at the encoding session (no interference condition) and the other half after a different mood induction (interference condition). Amongst participants for whom the MIP was effective, an emotional interference effect appeared only in the sleep-deprived condition, with a lower recall of word pairs subjected to contextual interference than of the other pairs. These findings support the hypothesis of a decoupling between memories and their "affective blanket" during post-learning sleep, protecting recent memories against emotional contextual interference.

Does recall after sleep-dependent memory consolidation reinstate sensitivity to retroactive interference?

Previous studies have shown that newly encoded memories are more resistant to retroactive interference when participants are allowed to sleep after learning the original material, suggesting a sleep-related strengthening of memories. In the present study, we investigated delayed, long-term effects of sleep vs. sleep deprivation (SD) on the first post-training night on memory consolidation and resistance to interference. On day 1, participants learned a list of unrelated word pairs (AB), either in the morning or in the evening, then spent the post-training night in a sleep or sleep deprivation condition, in a within-subject paradigm. On day 4, at the same time of day, they learned a novel list of word pairs (AC) in which 50% of the word pairs stemmed with the same word than in the AB list, resulting in retroactive interference. Participants had then to recall items from the AB list upon presentation of the "A" stem. Recall was marginally improved in the evening, as compared to the morning learning group. Most importantly, retroactive interference effects were found in the sleep evening group only, contrary to the hypothesis that sleep exerts a protective role against intrusion by novel but similar learning. We tentatively suggest that these results can be explained in the framework of the memory reconsolidation theory, stating that exposure to similar information sets back consolidated items in a labile form again sensitive to retroactive interference. In this context, sleep might not protect against interference but would promote an update of existing episodic memories while preventing saturation of the memory network due to the accumulation of dual traces.

MEG correlates of learning novel objects properties in children.

Learning the functional properties of objects is a core mechanism in the development of conceptual, cognitive and linguistic knowledge in children. The cerebral processes underlying these learning mechanisms remain unclear in adults and unexplored in children. Here, we investigated the neurophysiological patterns underpinning the learning of functions for novel objects in 10-year-old healthy children. Event-related fields (ERFs) were recorded using magnetoencephalography (MEG) during a picture-definition task. Two MEG sessions were administered, separated by a behavioral verbal learning session during which children learned short definitions about the "magical" function of 50 unknown non-objects. Additionally, 50 familiar real objects and 50 other unknown non-objects for which no functions were taught were presented at both MEG sessions. Children learned at least 75% of the 50 proposed definitions in less than one hour, illustrating children's powerful ability to rapidly map new functional meanings to novel objects. Pre- and post-learning ERFs differences were analyzed first in sensor then in source space. Results in sensor space disclosed a learning-dependent modulation of ERFs for newly learned non-objects, developing 500-800 msec after stimulus onset. Analyses in the source space windowed over this late temporal component of interest disclosed underlying activity in right parietal, bilateral orbito-frontal and right temporal regions. Altogether, our results suggest that learning-related evolution in late ERF components over those regions may support the challenging task of rapidly creating new semantic representations supporting the processing of the meaning and functions of novel objects in children.

Sleep may not benefit learning new phonological categories.

It is known that sleep participates in memory consolidation processes. However, results obtained in the auditory domain are inconsistent. Here we aimed at investigating the role of post-training sleep in auditory training and learning new phonological categories, a fundamental process in speech processing. Adult French-speakers were trained to identify two synthetic speech variants of the syllable /d∂/ during two 1-h training sessions. The 12-h interval between the two sessions either did (8 p.m. to 8 a.m. ± 1 h) or did not (8 a.m. to 8 p.m. ± 1 h) included a sleep period. In both groups, identification performance dramatically improved over the first training session, to slightly decrease over the 12-h offline interval, although remaining above chance levels. Still, reaction times (RT) were slowed down after sleep suggesting higher attention devoted to the learned, novel phonological contrast. Notwithstanding, our results essentially suggest that post-training sleep does not benefit more than wakefulness to the consolidation or stabilization of new phonological categories.

Selective modulations of attentional asymmetries after sleep deprivation.

Pseudoneglect is a slight but consistent misplacement of attention toward the left visual field, commonly observed in young healthy subjects. This leftward attentional bias is thought to result from a right hemispheric dominance in visuospatial processing. Changes in endogenous levels of alertness may modulate attentional asymmetries and pseudoneglect in particular. In line with this hypothesis, it has been shown that sleep deprived shift-workers present a reversal of their attentional bias in a landmark (LDM) task (Manly, T., Dobler, V. B., Dodds, C. M., & George, M. A. (2005). Rightward shift in spatial awareness with declining alertness. Neuropsychologia, 43(12), 1721-1728). However, circadian disturbances and fatigue effects at the end of a shift work may have contributed to this reversal effect. In a first experiment, we show that sleep deprivation (SD) under controlled conditions does not markedly change the leftward bias, observable both at 21:00 and at 07:00 after SD. In a second experiment, we tested the hypothesis that a drastic reduction or inversion in the attentional bias would be present only when both the circadian drive for sleep propensity is maximal (i.e. around 05:00) and homeostatic sleep pressure is high. Thus participants were tested at 21:00 and under SD conditions at 05:00 and 09:00. Additionally, we used the greyscales (GS) task well-known to evidence a leftward bias in luminance judgments. Although results evidenced a consistent leftward bias both in the LDM and GS, we found a suppression of the leftward bias at the circadian nadir of alertness (05:00) after SD only for the GS, but not for the LDM. Noticeably, the leftward bias in the GS vanished at 05:00 after SD but reappeared at 09:00 despite continued SD, suggesting a predominant circadian influence on attentional asymmetries in the GS. Additionally, inter-sessions correlations evidenced a reproducible, consistent bias both in the LDM and GS, with no consistent relationship between the two tasks, suggesting independence of the neural networks subtending performance in LDM and GS. Overall, our results suggest that SD per se does not impede the leftward bias both in LDM and GS, whereas circadian-related variations in vigilance may impact attentional asymmetries in luminance judgments.

Recurrent boosting effects of short inactivity delays on performance: an ERPs study.

BACKGROUND: Recent studies investigating off-line processes of consolidation in motor learning have demonstrated a sudden, short-lived improvement in performance after 5-30 minutes of post-training inactivity. Here, we investigated further this behavioral boost in the context of the probabilistic serial reaction time task, a paradigm of implicit sequence learning. We looked both at the electrophysiological correlates of the boost effect and whether this phenomenon occurs at the initial training session only. FINDINGS: Reaction times consistently improved after a 30-minute break within two sessions spaced four days apart, revealing the reproducibility of the boost effect. Importantly, this improvement was unrelated to the acquisition of the sequential regularities in the material. At both sessions, event-related potentials (ERPs) analyses disclosed a boost-associated increased amplitude of a first negative component, and shorter latencies for a second positive component. CONCLUSION: Behavioral and ERP data suggest increased processing fluency after short delays, which may support transitory improvements in attentional and/or motor performance and participate in the final setting up of the neural networks involved in the acquisition of novel skills.