James W. Antony

Cued memory reactivation during sleep influences skill learning.

Information acquired during waking can be reactivated during sleep, promoting memory stabilization. After people learned to produce two melodies in time with moving visual symbols, we enhanced relative performance by presenting one melody during an afternoon nap. Electrophysiological signs of memory processing during sleep corroborated the notion that appropriate auditory stimulation that does not disrupt sleep can nevertheless bias memory consolidation in relevant brain circuitry.

The Role of Memory Reactivation during Wakefulness and Sleep in Determining Which Memories Endure

Consolidation makes it possible for memories of our daily experiences to be stored in an enduring way. We propose that memory consolidation depends on the covert reactivation of previously learned material both during sleep and wakefulness. Here we tested whether the operation of covert memory reactivation influences the fundamental selectivity of memory storage—of all the events we experience each day, which will be retained and which forgotten? We systematically manipulated the value of information learned by 60 young subjects; they learned 72 object-location associations while hearing characteristic object sounds, and a number on each object indicated the reward value that could potentially be earned during a future memory test. Recall accuracy declined to a greater extent for low-value than for high-value associations after either a 90 min nap or a 90 min wake interval. Yet, via targeted memory reactivation of half of the low-value associations using the corresponding sounds, these memories were rescued from forgetting. Only cued associations were rescued when sounds were applied during wakefulness, whereas the entire set of low-value associations was rescued from forgetting when the manipulation occurred during sleep. The benefits accrued from presenting corresponding sounds show that covert reactivation is a major factor determining the selectivity of memory consolidation in these circumstances. By extension, covert reactivation may determine the ultimate fate of our memories, though wake and sleep reactivation might play distinct roles in this process, the former helping to strengthen individual, salient memories, and the latter strengthening, while also linking, categorically related memories together.

Unlearning implicit social biases during sleep

Sleep on it: Consolidating implicit learning A good nights sleep is one of the best ways to fix recently learned information into long-lasting memory. Recent evidence suggests that recent memories are reactivated during sleep and woven into existing representations of stored information. Hu et al. now demonstrate that triggering memory consolidation during sleep can help set into place recently learned anti-bias training (see the Perspective by Feld and Born). Changes in peoples stereotypical attitudes toward race and gender were maintained for up to 1 week after training. Science, this issue p. 1013; see also p. 971 People’s stereotypical associations can be reduced when training is combined with memory consolidation during sleep. [Also see Perspective by Feld and Born] Although people may endorse egalitarianism and tolerance, social biases can remain operative and drive harmful actions in an unconscious manner. Here, we investigated training to reduce implicit racial and gender bias. Forty participants processed counterstereotype information paired with one sound for each type of bias. Biases were reduced immediately after training. During subsequent slow-wave sleep, one sound was unobtrusively presented to each participant, repeatedly, to reactivate one type of training. Corresponding bias reductions were fortified in comparison with the social bias not externally reactivated during sleep. This advantage remained 1 week later, the magnitude of which was associated with time in slow-wave and rapid-eye-movement sleep after training. We conclude that memory reactivation during sleep enhances counterstereotype training and that maintaining a bias reduction is sleep-dependent.

Targeted Memory Reactivation during Sleep Depends on Prior Learning

STUDY OBJECTIVES When sounds associated with learning are presented again during slow-wave sleep, targeted memory reactivation (TMR) can produce improvements in subsequent location recall. Here we used TMR to investigate memory consolidation during an afternoon nap as a function of prior learning. PARTICIPANTS Twenty healthy individuals (8 male, 19-23 y old). MEASUREMENTS AND RESULTS Participants learned to associate each of 50 common objects with a unique screen location. When each object appeared, its characteristic sound was played. After electroencephalography (EEG) electrodes were applied, location recall was assessed for each object, followed by a 90-min interval for sleep. During EEG-verified slow-wave sleep, half of the sounds were quietly presented over white noise. Recall was assessed 3 h after initial learning. A beneficial effect of TMR was found in the form of higher recall accuracy for cued objects compared to uncued objects when pre-sleep accuracy was used as an explanatory variable. An analysis of individual differences revealed that this benefit was greater for participants with higher pre-sleep recall accuracy. In an analysis for individual objects, cueing benefits were apparent as long as initial recall was not highly accurate. Sleep physiology analyses revealed that the cueing benefit correlated with delta power and fast spindle density. CONCLUSIONS These findings substantiate the use of targeted memory reactivation (TMR) methods for manipulating consolidation during sleep. TMR can selectively strengthen memory storage for object-location associations learned prior to sleep, except for those near-perfectly memorized. Neural measures found in conjunction with TMR-induced strengthening provide additional evidence about mechanisms of sleep consolidation.

Fear not: manipulating sleep might help you forget

Memory storage is not static - updating is often needed. When it comes to traumatic memories, forgetting may be desired. Two innovative studies recently demonstrated that fear memories can be weakened during sleep using odors associated with fear-learning episodes. New strategies along these lines should be carefully considered for treating unwanted fears.

Using Oscillating Sounds to Manipulate Sleep Spindles

Introduction EEG oscillations known as sleep spindles have been linked with various aspects of cognition, but the specific functions they signal remain controversial. Two types of EEG sleep spindles have been distinguished: slow spindles at 11-13.5 Hz and fast spindles at 13.5-16 Hz. Slow spindles exhibit a frontal scalp topography, whereas fast spindles exhibit a posterior scalp topography and have been preferentially linked with memory consolidation during sleep. To advance understanding beyond that provided from correlative studies of spindles, we aimed to develop a new method to systematically manipulate spindles. Aims and Methods We presented repeating bursts of oscillating white noise to people during a 90-min afternoon nap. During stage 2 and slow-wave sleep, oscillations were embedded within contiguous 10-s stimulation intervals, each comprising 2 s of white noise amplitude modulated at 12 Hz (targeting slow spindles), 15 Hz (targeting fast spindles), or 50 Hz followed by 8 s of constant white noise. Results During oscillating stimulation compared to constant stimulation, parietal EEG recordings showed more slow spindles in the 12-Hz condition, more fast spindles in the 15-Hz condition, and no change in the 50-Hz control condition. These effects were topographically selective, and were absent in frontopolar EEG recordings, where slow spindle density was highest. Spindles during stimulation were similar to spontaneous spindles in standard physiological features, including duration and scalp distribution. Conclusions These results define a new method to selectively and noninvasively manipulate spindles through acoustic resonance, while also providing new evidence for functional distinctions between the 2 types of EEG spindles.

Hippocampal Contributions to Declarative Memory Consolidation During Sleep

The human brain faces a fundamental information storage challenge—forming useful new memories while not over-writing important old ones. Memory consolidation, and the corresponding interplay between the hippocampus and neocortex, is a protracted process to adjudicate between these two competing factors. Converging evidence from behavioral, cellular, and systems neuroscience strongly implicates a special role for sleep in stabilizing new declarative memories. In this chapter, we review evidence that during sleep the reactivation of newly acquired neuronal traces has lasting implications for memory transformation and stabilization. We first summarize relevant theoretical issues in memory research and then outline the physiological properties of sleep that may allow for this reactivation. We consider many factors that affect spontaneous memory reactivation, and we highlight research showing that memories can be selectively targeted and modified using learning-related stimuli. Ultimately, the ability to rescue otherwise fleeting episodes from oblivion plays a vital role in human life. Research elucidating this ability will also be critical for understanding how memory breaks down in aging and disease.

Competitive learning modulates memory consolidation during sleep

&NA; Competition between memories can cause weakening of those memories. Here we investigated memory competition during sleep in human participants by presenting auditory cues that had been linked to two distinct picture‐location pairs during wake. We manipulated competition during learning by requiring participants to rehearse picture‐location pairs associated with the same sound either competitively (choosing to rehearse one over the other, leading to greater competition) or separately; we hypothesized that greater competition during learning would lead to greater competition when memories were cued during sleep. With separate‐pair learning, we found that cueing benefited spatial retention. With competitive‐pair learning, no benefit of cueing was observed on retention, but cueing impaired retention of well‐learned pairs (where we expected strong competition). During sleep, post‐cue beta power (16–30 Hz) indexed competition and predicted forgetting, whereas sigma power (11–16 Hz) predicted subsequent retention. Taken together, these findings show that competition between memories during learning can modulate how they are consolidated during sleep.

Targeted memory reactivation during sleep elicits neural signals related to learning content

Reactivation of learning-related neural activity patterns is thought to drive memory stabilization. However, finding reliable, non-invasive, content-specific indicators of reactivation remains a central challenge. Here, we attempted to decode the content of reactivated memories in the electroencephalogram (EEG) during sleep. During encoding, human participants learned to associate spatial locations of visual objects with left- or right-hand movements, and each object was accompanied by an inherently related sound. During subsequent slow-wave sleep within an afternoon nap, we presented half of the sound cues that were associated (during wake) with left- and right-hand movements before bringing participants back for a final post-nap test. We trained a classifier on sleep EEG data (focusing on lateralized EEG features that discriminated left- vs. right-sided trials during wake) to predict learning content when we reactivated the memories during sleep. Discrimination performance was significantly above chance and predicted subsequent memory, supporting the idea that reactivation leads to memory stabilization. Moreover, these lateralized signals increased with post-cue spindle power, demonstrating that reactivation has a strong relationship with spindles. These results show that lateralized activity related to individual memories can be decoded from sleep EEG, providing an effective indicator of offline reactivation.

Retrieval and sleep both counteract the forgetting of spatial information

Repeatedly studying information is a good way to strengthen memory storage. Nevertheless, testing recall often produces superior long-term retention. Demonstrations of this testing effect, typically with verbal stimuli, have shown that repeated retrieval through testing reduces forgetting. Sleep also benefits memory storage, perhaps through repeated retrieval as well. That is, memories may generally be subject to forgetting that can be counteracted when memories become reactivated, and there are several types of reactivation: (i) via intentional restudying, (ii) via testing, (iii) without provocation during wake, or (iv) during sleep. We thus measured forgetting for spatial material subjected to repeated study or repeated testing followed by retention intervals with sleep versus wake. Four groups of subjects learned a set of visual object-location associations and either restudied the associations or recalled locations given the objects as cues. We found the advantage for restudied over retested information was greater in the PM than AM group. Additional groups tested at 5-min and 1-wk retention intervals confirmed previous findings of greater relative benefits for restudying in the short-term and for retesting in the long-term. Results overall support the conclusion that repeated reactivation through testing or sleeping stabilizes information against forgetting.