Developmental changes in retention and generalization of nonadjacent dependencies over a period containing sleep in 18-mo-old infants.

Sleep promotes the stabilization of memories in adulthood, with a growing literature on the benefits of sleep for memory in infants and children. In two studies, we examined the role of sleep in the retention and generalization of nonadjacent dependencies (NADs; e.g., a-X-b/c-X-d phrases) in an artificial language. Previously, a study demonstrated that over a delay of 4 h, 15 mo olds who nap after training retain a general memory of the NAD rule instead of memory for specific NADs heard during training. In experiment 1, we designed a replication of the nap condition used in the earlier study but tested 18-mo-old infants. Infants of this age retained veridical memory for specific NADs over a delay containing sleep, providing preliminary evidence of the development of memory processes (experiment 1). In experiment 2, we tested 18 mo olds' ability to generalize the NAD to new vocabulary, finding only infants who napped after training generalized their knowledge of the pattern to completely novel phrases. Overall, by 18 mo of age, children retain specific memories over a period containing sleep, and sleep promotes abstract memories to a greater extent than wakefulness.

The Role of Sleep in Retention of New Words in Habitually and Non-Habitually Napping Children.

Daytime napping contributes to retention of new word learning in children. Importantly, children transition out of regular napping between ages 3-5 years, and the impact of this transition on memory is unclear. Here, we examined the performance of both non-habitually napping children (nap 0-3 days per week, n = 28) and habitually napping children (nap 4-7 days per week, n = 30) on a word learning task after a delay including either sleep or wakefulness. Children ages 3.5-4.5 years old experienced a brief exposure to two novel labels and their referents during training, a scenario that replicates learning experiences children encounter every day. After a 4-h delay, children were tested on the object-label associations. Using mixed effects logistic regression, we compared retention performance. Non-habitual nappers and habitual nappers displayed a different pattern of retention such that non-habitually napping children did equally well on a test of retention regardless of whether they napped or stayed awake during the delay. In contrast, habitually napping children needed a nap after learning to retain the novel object-label associations 4 h later. As a group, habitual nappers who remained awake after learning performed no better than chance on the retention test. As children transition out of naps, they may be less susceptible to interference and are better able to retain newly learned words across a delay including wakefulness.

A daytime nap combined with nighttime sleep promotes learning in toddlers.

Napping after learning promotes consolidation of new information during infancy. Yet, whether naps play a similar role during toddlerhood, a stage when many children are beginning to transition away from napping, is less clear. In Experiment 1, we examined whether napping after learning promotes generalization of novel category exemplars 24 h later. Young children (N = 54, age range = 29-36 months) viewed three category exemplars in different contexts from each of three categories and remained awake (No-Nap condition) or napped (Nap condition) after encoding and were then tested 24 h later. Children who napped after learning showed superior generalization 24 h later relative to children who did not nap. In a Nap-Control condition tested 4 h after awakening from a nap, children performed at the same low level as in the No-Nap condition, indicating that generalization stemmed from an additional period of nighttime sleep and not simply from a nap or increased time. In Experiment 2, we examined whether nighttime sleep is sufficient for generalization if it occurs soon after learning. An additional group of children (N = 18) learned before bedtime and were tested 4 h after waking up the next day. Children did not generalize as well as those who had a nap combined with subsequent nighttime sleep. These findings suggest that naps, when combined with a period of nighttime sleep, might help toddlers to retain newly learned information and lead to delayed benefits in generalization.

Exploring the "anchor word" effect in infants: Segmentation and categorisation of speech with and without high frequency words.

High frequency words play a key role in language acquisition, with recent work suggesting they may serve both speech segmentation and lexical categorisation. However, it is not yet known whether infants can detect novel high frequency words in continuous speech, nor whether they can use them to help learning for segmentation and categorisation at the same time. For instance, when hearing "you eat the biscuit", can children use the high-frequency words "you" and "the" to segment out "eat" and "biscuit", and determine their respective lexical categories? We tested this in two experiments. In Experiment 1, we familiarised 12-month-old infants with continuous artificial speech comprising repetitions of target words, which were preceded by high-frequency marker words that distinguished the targets into two distributional categories. In Experiment 2, we repeated the task using the same language but with additional phonological cues to word and category structure. In both studies, we measured learning with head-turn preference tests of segmentation and categorisation, and compared performance against a control group that heard the artificial speech without the marker words (i.e., just the targets). There was no evidence that high frequency words helped either speech segmentation or grammatical categorisation. However, segmentation was seen to improve when the distributional information was supplemented with phonological cues (Experiment 2). In both experiments, exploratory analysis indicated that infants' looking behaviour was related to their linguistic maturity (indexed by infants' vocabulary scores) with infants with high versus low vocabulary scores displaying novelty and familiarity preferences, respectively. We propose that high-frequency words must reach a critical threshold of familiarity before they can be of significant benefit to learning.

Parameters of Memory Reconsolidation: Learning Mode Influences Likelihood of Memory Modification.

When previously consolidated hippocampally dependent memory traces are reactivated they enter a vulnerable state in which they can be altered with new information, after which they must be re-consolidated in order to restabilize the trace. The existing body of literature on episodic reconsolidation largely focuses on the when and how of successful memory reactivation. What remains poorly understood is how the nature of newly presented information affects the likelihood of a vulnerable episodic memory being altered. We used our episodic memory reconsolidation paradigm to investigate if the intention to encode impacts what subsequently becomes attributed to an older, reactivated memory. Participants learned two lists of objects separated by 48 h. We integrated a modified item-list directed-forgetting paradigm into the encoding of the second object list by cueing participants to learn some of the objects intentionally (intentional learning), while other objects were presented without a cue (incidental learning). Under conditions of memory reactivation, subjects showed equal rates of memory modification for intentionally- and incidentally-learned objects. However, in the absence of reactivation we observed high misattribution rates of incidentally-learned objects. We consider two interpretations of these data, with contrasting implications for understanding the conditions that influence memory malleability, and suggest further work that should help decide between them.

Associations between sleep and episodic memory updating.

Prior research shows that contextual reminders can reactivate hippocampal links to previously consolidated memories, rendering them susceptible to being updated with new information which then is reconsolidated. Studies implicate sleep in the reconsolidation of reactivated memories, but it is unknown what role sleep plays in updating of a previously consolidated trace with new information. We tracked participants' sleep during an episodic reconsolidation paradigm, first with actigraphy (Experiment 1) then with polysomnography (Experiment 2). Our paradigm involved two learning sessions and a retrieval session, each separated by 48 hr. We reminded participants of the first learning experience immediately prior to the second, which led them to update the earlier memory with elements of the later experience. In Experiment 1, less sleep after Session 1 and more sleep after Session 2 are associated with increased updating. In Experiment 2, N2 sleep spindles (SSs) after the reminder and new learning are associated with more updating, but primarily when spindle activity after Session 1 is low. Thus, total sleep time and N2 SSs contribute to sleep-dependent updating of episodic memory. This outcome is consistent with other work connecting SS activity to the integration of novel information into existing knowledge structures, extended here with the study of how variations in sleep over successive nights contribute to this process. We discuss some possible roles of spindles in the decontextualization of hippocampal memory over time. Although much work addresses the role of sleep in the consolidation of new memories, this work uniquely addresses the contribution of sleep to the updating of a previously consolidated trace with new information.

REM sleep in naps differentially relates to memory consolidation in typical preschoolers and children with Down syndrome.

Sleep is recognized as a physiological state associated with learning, with studies showing that knowledge acquisition improves with naps. Little work has examined sleep-dependent learning in people with developmental disorders, for whom sleep quality is often impaired. We examined the effect of natural, in-home naps on word learning in typical young children and children with Down syndrome (DS). Despite similar immediate memory retention, naps benefitted memory performance in typical children but hindered performance in children with DS, who retained less when tested after a nap, but were more accurate after a wake interval. These effects of napping persisted 24 h later in both groups, even after an intervening overnight period of sleep. During naps in typical children, memory retention for object-label associations correlated positively with percent of time in rapid eye movement (REM) sleep. However, in children with DS, a population with reduced REM, learning was impaired, but only after the nap. This finding shows that a nap can increase memory loss in a subpopulation, highlighting that naps are not universally beneficial. Further, in healthy preschooler's naps, processes in REM sleep may benefit learning.

Curiosity-driven memory enhancement persists over time but does not benefit from post-learning sleep.

Sleep-dependent memory processing is dependent on several factors at learning, including emotion, encoding strength, and knowledge of future relevance. Recent work documents the role of curiosity on learning, showing that memory associated with high-curiosity encoding states is retained better and that this effect may be driven by activity within the dopaminergic circuit. Here, we examined whether this curiosity effect was enhanced by or dependent on sleep-related consolidation. Participants learned the answers to trivia questions that they had previously rated on a curiosity scale, and they were shown faces between each question and answer presentation. Memory for these answers and faces was tested either immediately or after a 12-hour delay containing sleep or wakefulness, and polysomnography data was collected for a subset of the sleep participants. Although the curiosity effect for both the answers and incidentally-learned faces was replicated in immediate tests and after the 12-hour delay, the effect was not impacted by the presence of sleep in either case, nor did the effect show a relationship with total sleep time or time in slow-wave sleep. This study suggests that curiosity may be a learning factor that is not subsequently affected by sleep-dependent memory consolidation, but more work ought to examine the role of sleep on curiosity-driven memory in other contexts.

Learning Without Trying: The Clinical Relevance of Statistical Learning.

Purpose: Statistical learning research seeks to identify the means by which learners, with little perceived effort, acquire the complexities of language. In the past 50 years, numerous studies have uncovered powerful learning mechanisms that allow for learning within minutes of exposure to novel language input. Method: We consider the value of information from statistical learning studies that show potential for making treatment of language disorders faster and more effective. Results: Available studies include experimental research that demonstrates the conditions under which rapid learning is possible, research showing that these findings apply to individuals with disorders, and translational work that has applied learning principles in treatment and educational contexts. In addition, recent research on memory formation has implications for treatment of language deficits. Conclusion: The statistical learning literature offers principles for learning that can improve clinical outcomes for children with language impairment. There is potential for further applications of this basic research that is yet unexplored.

How who is talking matters as much as what they say to infant language learners.

Human vocalizations contain both voice characteristics that convey who is talking and sophisticated linguistic structure. Inter-talker variation in voice characteristics is traditionally seen as posing a challenge for infant language learners, who must disregard this variation when the task is to detect talkers' shared linguistic conventions. However, talkers often differ markedly in their pronunciation, vocabulary, and grammar. This is true even in monolingual environments, given factors like gender, dialect, and proficiency. We therefore asked whether infants treat the voice characteristics distinguishing talkers as a cue for learning linguistic conventions that one talker may follow more closely than another. Supporting this previously untested hypothesis, 12-month-olds did not freely combine two talkers' sentences distinguished by voice to more robustly learn the talkers' shared grammar rules. Rather, they used this voice information to learn rules to which only one talker adhered, a finding replicated in same-aged infants with greater second language exposure. Both language groups generalized the rules to novel sentences produced by a novel talker. Voice characteristics can thus help infants learn and generalize talker-dependent linguistic structure, which pervades natural language. Results are interpreted in light of theories linking language learning with voice perception.

Losing memories during sleep after targeted memory reactivation.

Targeting memories during sleep opens powerful and innovative ways to influence the mind. We used targeted memory reactivation (TMR), which to date has been shown to strengthen learned episodes, to instead induce forgetting (TMR-Forget). Participants were first trained to associate the act of forgetting with an auditory forget tone. In a second, separate, task they learned object-sound-location pairings. Shortly thereafter, some of the object sounds were played during slow wave sleep, paired with the forget tone to induce forgetting. One week later, participants demonstrated lower recall of reactivated versus non-reactivated objects and impaired recognition memory and lowered confidence for the spatial location of the reactivated objects they failed to spontaneously recall. The ability to target specific episodic memories for forgetting during sleep has implications for developing novel therapeutic techniques for psychological disorders such as PTSD and phobias.

Brain correlates of memory reconsolidation: A role for the TPJ.

In this paper, we investigate the process by which new experiences reactivate and potentially update old memories. Such memory reconsolidation appears dependent on the extent to which current experience deviates from what is predicted by the reactivated memory (i.e. prediction error). If prediction error is low, the reactivated memory is likely to be updated with new information. If it is high, however, a new, separate, memory is more likely to be formed. The temporal parietal junction TPJ has been shown across a broad range of content areas (attention, social cognition, decision making and episodic memory) to be sensitive to the degree to which current information violates the observer's expectations - in other words, prediction error. In the current paper, we investigate whether the level of TPJ activation during encoding predicts if the encoded information will be used to form a new memory or update a previous memory. We find that high TPJ activation predicts new memory formation. In a secondary analysis, we examine whether reactivation strength - which we assume leads to a strong memory-based prediction - mediates the likelihood that a given individual will use new information to form a new memory rather than update a previous memory. Individuals who strongly reactivate previous memories are less likely to update them than individuals who weakly reactivate them. We interpret this outcome as indicating that strong predictions lead to high prediction error, which favors new memory formation rather than updating of a previous memory.

Words to Sleep On: Naps Facilitate Verb Generalization in Habitually and Nonhabitually Napping Preschoolers.

A nap soon after encoding leads to better learning in infancy. However, whether napping plays the same role in preschoolers' learning is unclear. In Experiment 1 (N = 39), 3-year-old habitual and nonhabitual nappers learned novel verbs before a nap or a period of wakefulness and received a generalization test examining word extension to novel actors after 24 hr. Only habitual and nonhabitual nappers who napped after learning generalized 24 hr later. In Experiment 2 (N = 40), children learned the same verbs but were tested within 2-3 min of training. Here, habitual and nonhabitual nappers retained the mappings but did not generalize. The results suggest that naps consolidate weak learning that habitual and nonhabitual nappers would otherwise forget over periods of wakefulness.

Sleep confers a benefit for retention of statistical language learning in 6.5month old infants.

Infants show robust ability to track transitional probabilities within language and can use this information to extract words from continuous speech. The degree to which infants remember these words across a delay is unknown. Given well-established benefits of sleep on long-term memory retention in adults, we examine whether sleep similarly facilitates memory in 6.5month olds. Infants listened to an artificial language for 7minutes, followed by a period of sleep or wakefulness. After a time-matched delay for sleep and wakefulness dyads, we measured retention using the head-turn-preference procedure. Infants who slept retained memory for the extracted words that was prone to interference during the test. Infants who remained awake showed no retention. Within the nap group, retention correlated with three electrophysiological measures (1) absolute theta across the brain, (2) absolute alpha across the brain, and (3) greater fronto-central slow wave activity (SWA).

Do infants retain the statistics of a statistical learning experience? Insights from a developmental cognitive neuroscience perspective.

Statistical structure abounds in language. Human infants show a striking capacity for using statistical learning (SL) to extract regularities in their linguistic environments, a process thought to bootstrap their knowledge of language. Critically, studies of SL test infants in the minutes immediately following familiarization, but long-term retention unfolds over hours and days, with almost no work investigating retention of SL. This creates a critical gap in the literature given that we know little about how single or multiple SL experiences translate into permanent knowledge. Furthermore, different memory systems with vastly different encoding and retention profiles emerge at different points in development, with the underlying memory system dictating the fidelity of the memory trace hours later. I describe the scant literature on retention of SL, the learning and retention properties of memory systems as they apply to SL, and the development of these memory systems. I propose that different memory systems support retention of SL in infant and adult learners, suggesting an explanation for the slow pace of natural language acquisition in infancy. I discuss the implications of developing memory systems for SL and suggest that we exercise caution in extrapolating from adult to infant properties of SL.This article is part of the themed issue 'New frontiers for statistical learning in the cognitive sciences'.

Preschool Children's Memory for Word Forms Remains Stable Over Several Days, but Gradually Decreases after 6 Months.

Research on word learning has focused on children's ability to identify a target object when given the word form after a minimal number of exposures to novel word-object pairings. However, relatively little research has focused on children's ability to retrieve the word form when given the target object. The exceptions involve asking children to recall and produce forms, and children typically perform near floor on these measures. In the current study, 3- to 5-year-old children were administered a novel test of word form that allowed for recognition memory and manual responses. Specifically, when asked to label a previously trained object, children were given three forms to choose from: the target, a minimally different form, and a maximally different form. Children demonstrated memory for word forms at three post-training delays: 10 mins (short-term), 2-3 days (long-term), and 6 months to 1 year (very long-term). However, children performed worse at the very long-term delay than the other time points, and the length of the very long-term delay was negatively related to performance. When in error, children were no more likely to select the minimally different form than the maximally different form at all time points. Overall, these results suggest that children remember word forms that are linked to objects over extended post-training intervals, but that their memory for the forms gradually decreases over time without further exposures. Furthermore, memory traces for word forms do not become less phonologically specific over time; rather children either identify the correct form, or they perform at chance.

The extended trajectory of hippocampal development: Implications for early memory development and disorder.

Hippocampus has an extended developmental trajectory, with refinements occurring in the trisynaptic circuit until adolescence. While structural change should suggest a protracted course in behavior, some studies find evidence of precocious hippocampal development in the first postnatal year and continuity in memory processes beyond. However, a number of memory functions, including binding and relational inference, can be cortically supported. Evidence from the animal literature suggests that tasks often associated with hippocampus (visual paired comparison, binding of a visuomotor response) can be mediated by structures external to hippocampus. Thus, a complete examination of memory development will have to rule out cortex as a source of early memory competency. We propose that early memory must show properties associated with full function of the trisynaptic circuit to reflect "adult-like" memory function, mainly (1) rapid encoding of contextual details of overlapping patterns, and (2) retention of these details over sleep-dependent delays. A wealth of evidence suggests that these functions are not apparent until 18-24 months, with behavioral discontinuities reflecting shifts in the neural structures subserving memory beginning approximately at this point in development. We discuss the implications of these observations for theories of memory and for identifying and measuring memory function in populations with typical and atypical hippocampal function.

Sleep as a window into early neural development: Shifts in sleep-dependent learning effects across early childhood.

Sleep is an important physiological state for the consolidation and generalization of new learning in children and adults. We review the literature on sleep-dependent memory consolidation and generalization in infants and preschool children and place the findings in the context of the development of the neural systems underlying memory (hippocampus and its connections to cortex). Based on the extended trajectory of hippocampal development, transitions in the nature of sleep-dependent learning are expected. The studies reviewed here show shifts in the nature of sleep-dependent learning across early childhood, with sleep facilitating generalization in infants but enhancing precise memory after 18-24 months of age. Future studies on sleep-dependent learning in infants and young children must take these transitions in early brain development into account.

Does hearing two dialects at different times help infants learn dialect-specific rules?

Infants might be better at teasing apart dialects with different language rules when hearing the dialects at different times, since language learners do not always combine input heard at different times. However, no previous research has independently varied the temporal distribution of conflicting language input. Twelve-month-olds heard two artificial language streams representing different dialects-a "pure stream" whose sentences adhered to abstract grammar rules like aX bY, and a "mixed stream" wherein any a- or b-word could precede any X- or Y-word. Infants were then tested for generalization of the pure stream's rules to novel sentences. Supporting our hypothesis, infants showed generalization when the two streams' sentences alternated in minutes-long intervals without any perceptually salient change across streams (Experiment 2), but not when all sentences from these same streams were randomly interleaved (Experiment 3). Results are interpreted in light of temporal context effects in word learning.