An Enduring Role for Hippocampal Pattern Completion in Addition to an Emergent Nonhippocampal Contribution to Holistic Episodic Retrieval after a 24†h Delay.

Episodic memory retrieval is associated with the holistic neocortical reinstatement of all event information, an effect driven by hippocampal pattern completion. However, whether holistic reinstatement occurs, and whether hippocampal pattern completion continues to drive reinstatement, after a period of consolidation is unclear. Theories of systems consolidation predict either a time-variant or time-invariant role of the hippocampus in the holistic retrieval of episodic events. Here, we assessed whether episodic events continue to be reinstated holistically and whether hippocampal pattern completion continues to facilitate holistic reinstatement following a period of consolidation. Female and male human participants learned "events" that comprised multiple overlapping pairs of event elements (e.g., person-location, object-location, location-person). Importantly, encoding occurred either immediately before or 24 h before retrieval. Using fMRI during the retrieval of events, we show evidence for holistic reinstatement, as well as a correlation between reinstatement and hippocampal pattern completion, regardless of whether retrieval occurred immediately or 24 h after encoding. Thus, hippocampal pattern completion continues to contribute to holistic reinstatement after a delay. However, our results also revealed that some holistic reinstatement can occur without evidence for a corresponding signature of hippocampal pattern completion after a delay (but not immediately after encoding). We therefore show that hippocampal pattern completion, in addition to a nonhippocampal process, has a role in holistic reinstatement following a period of consolidation. Our results point to a consolidation process where the hippocampus and neocortex may work in an additive, rather than compensatory, manner to support episodic memory retrieval.

Sleep bolsters schematically incongruent memories.

Our ability to recall memories is improved when sleep follows learning, suggesting that sleep facilitates memory consolidation. A number of factors are thought to influence the impact of sleep on newly learned information, such as whether or not we rehearse that information (e.g. via restudy or retrieval practice), or the extent to which the information is consistent with our pre-existing schematic knowledge. In this pre-registered, online study, we examined the effects of both rehearsal and schematic congruency on overnight consolidation. Participants learned noun-colour pairings (e.g. elephant-red) and rated each pairing as plausible or implausible before completing a baseline memory assessment. Afterwards, participants engaged in a period of restudy or retrieval practice for the pairings, and then entered a 12 h retention interval of overnight sleep or daytime wakefulness. Follow-up assessments were completed immediately after sleep or wake, and again 24 h after learning. Our data indicated that overnight consolidation was amplified for restudied relative to retested noun-colour pairings, but only when sleep occurred soon after learning. Furthermore, whereas plausible (i.e. schematically congruent) pairings were generally better remembered than implausible (i.e. schematically incongruent) pairings, the benefits of sleep were stronger for implausible relative to plausible memories. These findings challenge the notion that schema-conformant memories are preferentially strengthened during post-learning sleep.

Future-relevant memories are not selectively strengthened during sleep.

Overnight consolidation processes are thought to operate in a selective manner, such that important (i.e. future-relevant) memories are strengthened ahead of irrelevant information. Using an online protocol, we sought to replicate the seminal finding that the memory benefits of sleep are enhanced when people expect a future test [Wilhelm et al., 2011]. Participants memorised verbal paired associates to a criterion of 60 percent (Experiment 1) or 40 percent correct (Experiment 2) before a 12-hour delay containing overnight sleep (sleep group) or daytime wakefulness (wake group). Critically, half of the participants were informed that they would be tested again the following day, whereas the other half were told that they would carry out a different set of tasks. We observed a robust memory benefit of overnight consolidation, with the sleep group outperforming the wake group in both experiments. However, knowledge of an upcoming test had no impact on sleep-associated consolidation in either experiment, suggesting that overnight memory processes were not enhanced for future-relevant information. These findings, together with other failed replication attempts, show that sleep does not provide selective support to memories that are deemed relevant for the future.

Losing Control: Sleep Deprivation Impairs the Suppression of Unwanted Thoughts.

Unwanted memories often enter conscious awareness when individuals confront reminders. People vary widely in their talents at suppressing such memory intrusions; however, the factors that govern suppression ability are poorly understood. We tested the hypothesis that successful memory control requires sleep. Following overnight sleep or total sleep deprivation, participants attempted to suppress intrusions of emotionally negative and neutral scenes when confronted with reminders. The sleep-deprived group experienced significantly more intrusions (unsuccessful suppressions) than the sleep group. Deficient control over intrusive thoughts had consequences: Whereas in rested participants suppression reduced behavioral and psychophysiological indices of negative affect for aversive memories, it had no such salutary effect for sleep-deprived participants. Our findings raise the possibility that sleep deprivation disrupts prefrontal control over medial temporal lobe structures that support memory and emotion. These data point to an important role of sleep disturbance in maintaining and exacerbating psychiatric conditions characterized by persistent, unwanted thoughts.

Phase-locked auditory stimulation of theta oscillations during rapid eye movement sleep.

Auditory closed-loop stimulation is a non-invasive technique that has been widely used to augment slow oscillations during non-rapid eye movement sleep. Based on the principles of closed-loop stimulation, we developed a novel protocol for manipulating theta activity (3-7 Hz) in rapid eye movement (REM) sleep. Sixteen healthy young adults were studied in two overnight conditions: Stimulation and Sham. In the Stimulation condition, 1 s of 5 Hz amplitude-modulated white noise was delivered upon detection of two supra-threshold theta cycles throughout REM sleep. In the Sham condition, corresponding time points were marked but no stimulation was delivered. Auditory stimulation entrained EEG activity to 5 Hz and evoked a brief (~0.5 s) increase in theta power. Interestingly, this initial theta surge was immediately followed by a prolonged (~3 s) period of theta suppression. Stimulation also induced a prolonged (~2 s) increase in beta power. Our results provide the first demonstration that the REM sleep theta rhythm can be manipulated in a targeted manner via auditory stimulation. Accordingly, auditory stimulation might offer a fruitful avenue for investigating REM sleep electrophysiology and its relationship to behavior.

Sleep deprivation induces fragmented memory loss.

Sleep deprivation increases rates of forgetting in episodic memory. Yet, whether an extended lack of sleep alters the qualitative nature of forgetting is unknown. We compared forgetting of episodic memories across intervals of overnight sleep, daytime wakefulness, and overnight sleep deprivation. Item-level forgetting was amplified across daytime wakefulness and overnight sleep deprivation, as compared to sleep. Importantly, however, overnight sleep deprivation led to a further deficit in associative memory that was not observed after daytime wakefulness. These findings suggest that sleep deprivation induces fragmentation among item memories and their associations, altering the qualitative nature of episodic forgetting.

Sleep Preserves Physiological Arousal in Emotional Memory.

Traumatic experiences are associated with increased emotional arousal. Overnight consolidation strengthens the episodic content of emotional memories, but it is still unclear how sleep influences the associated arousal response. To investigate this question, we compared the effects of sleep and wake on psychophysiological and subjective reactivity during emotional memory retrieval. Participants provided affective ratings for negative and neutral images while heart rate deceleration (HRD) and skin conductance responses (SCRs) were monitored. Following a 12-hour delay of sleep or wakefulness, participants completed an image recognition task where HRD, SCRs and affective ratings were recorded again. HRD responses to previously-encoded ("old") negative images were preserved after sleep but diminished after wakefulness. No between-group difference in HRD was observed for novel negative images at recognition, indicating that the effects of sleep for old images were not driven by a generalised overnight increase in visceral activity, or circadian factors. No significant effects of sleep were observed for SCRs or subjective ratings. Our data suggest that cardiac arousal experienced at the time of encoding is sensitive to plasticity-promoting processes during sleep in a similar manner to episodic aspects of emotional memory.

No effect of targeted memory reactivation during slow-wave sleep on emotional recognition memory.

Recent work has suggested that the benefits of sleep for memory consolidation are enhanced for highly salient (versus non-salient) memories. Using a technique known as targeted memory reactivation, it is possible to selectively strengthen newly learned memories by re-exposing the sleeping brain to auditory cues. The aim of the current study was to examine whether emotionally salient memories are also more responsive to targeted memory reactivation in slow-wave sleep than neutral memories. In an initial training phase, participants memorised emotionally negative and neutral pictures, which were each paired with a semantically related sound. Recognition for the pictures was assessed before and after a 90-min nap opportunity, during which half the sounds were re-presented during slow-wave sleep (as assessed via online polysomnographic sleep monitoring). We observed no effect of targeted memory reactivation on the recognition of emotionally negative or neutral memories. Our results highlight the importance of the memory paradigm used to assess targeted memory reactivation, and suggest that the robust and durable nature of recognition memory may make it an insensitive measure of behavioural targeted memory reactivation benefits. To fully assess the impacts of targeted memory reactivation on emotional memory processing in sleep, future studies should adopt experimental paradigms that maximise the salience of emotional stimuli while also providing a sensitive index of memory accuracy.

A role for consolidation in cross-modal category learning.

The ability to categorize objects and events is a fundamental human skill that depends upon the representation of multimodal conceptual knowledge. This study investigated the acquisition and consolidation of categorical information that required participants to integrate information across visual and auditory dimensions. The impact of wake- and sleep-dependent consolidation was investigated using a paradigm in which training and testing were separated by a delay spanning either an evening of sleep or daytime wakefulness, with a paired-associate episodic memory task used as a measure of classic sleep-dependent consolidation. Participants displayed good evidence of category learning, but did not show any wake- or sleep-dependent changes in memory for category information immediately following the delay. This is in contrast to paired-associate learning, where a sleep-dependent benefit was observed in memory recall. To replicate real-world concept learning, in which knowledge is acquired across multiple distinct episodes, participants were given a second opportunity for category learning following the consolidation delay. Here we found an interaction between consolidation and learning; with greater improvements in category knowledge as a result of the second learning session for those participants who had a sleep-filled delay. These results suggest a role for sleep in the consolidation of recently acquired categorical knowledge; however this benefit does not emerge as an immediate benefit in memory recall, but by enhancing the effectiveness of future learning. This study therefore provides insights into the processes responsible for the formation and development of conceptual representations.