Encoding colors and tones into working memory concurrently: A developmental investigation.

Working memory serves as a means to accumulate information and reorganize it. Researchers have long assumed that the natural organization of information is one stream at a time. This logic leads to the expectation that, when two different series of stimuli are to be remembered, performance should be superior if the series are presented one before the other in succession, rather than concurrently. Moreover, different accounts of attentional limits lead to different expectations for the change in the ability to encode two sets across age groups in childhood. Testing children from first grade (6-7 years) to adulthood, we presented sequences of colored objects and tones in succession or concurrently (with one color accompanying an unrelated tone) and found that performance was equally good no matter which presentation method was used. The results for both presentation methods closely matched the intricate pattern of development observed by Cowan et al. (2018), who used successive presentation only. We found marked developmental improvement in the ability to retain materials in each modality without an increasing cost of attention-sharing between modalities. Humans at least from the elementary school years through young adulthood thus display an ability to accommodate and organize two concurrent streams of information. RESEARCH HIGHLIGHTS: Memory for stimuli from multiple modalities is relevant to school performance and learning; here we investigate how attention is shared between remembering colors and tones. Participants received four colors and/or four tones for subsequent recognition on a trial, with dual modalities presented successively (0.5 s per stimulus) or concurrently (0.5 s per pair). Successive versus concurrent presentation had little effect on recognition, and the marked increase in memory performance with age did not come from dividing attention during encoding or maintenance. Children as young as first grade thus can encode and organize for later recognition colors and concurrently-presented, but unrelated, tones.

Expression of the monocarboxylate transporter MCT1 is required for virus-specific mouse CD8+ T cell memory development.

Lactate-proton symporter monocarboxylate transporter 1 (MCT1) facilitates lactic acid export from T cells. Here, we report that MCT1 is mandatory for the development of virus-specific CD8+ T cell memory. MCT1-deficient T cells were exposed to acute pneumovirus (pneumonia virus of mice, PVM) or persistent γ-herpesvirus (Murid herpesvirus 4, MuHV-4) infection. MCT1 was required for the expansion of virus-specific CD8+ T cells and the control of virus replication in the acute phase of infection. This situation prevented the subsequent development of virus-specific T cell memory, a necessary step in containing virus reactivation during γ-herpesvirus latency. Instead, persistent active infection drove virus-specific CD8+ T cells toward functional exhaustion, a phenotype typically seen in chronic viral infections. Mechanistically, MCT1 deficiency sequentially impaired lactic acid efflux from activated CD8+ T cells, caused an intracellular acidification inhibiting glycolysis, disrupted nucleotide synthesis in the upstream pentose phosphate pathway, and halted cell proliferation which, ultimately, promoted functional CD8+ T cell exhaustion instead of memory development. Taken together, our data demonstrate that MCT1 expression is mandatory for inducing T cell memory and controlling viral infection by CD8+ T cells.

Children's and adults' memory for the order of events in a museum: A preliminary study about temporal memory and its development using photo-taking and event-related potentials.

Remembering personal past events and their order is important. These capacities are essential to episodic and autobiographical memory theories, are needed in the creation of life stories and vital in forensic settings. As important as memory for events and their order are, relatively little is known about their development and the underlying neural processes that support them. Further, there is a paucity of studies that have examined memory and its development for autobiographical, yet controlled, events. The objective of this study was to examine memory for the temporal order of naturalistic "real world" events by directly comparing 7-11-year-olds and adults using both behavioral and event-related potential (ERP) measures. Participants photographed events at a local museum and after a delay, we used their photographs to test their memory for the temporal order of pairs of the events. We experimentally manipulated the temporal distance between the event pairs (whether the two events photographed in the pair had a short or long temporal distance between them). A memory asymmetry manipulation was also included such that at retrieval, photographs were either presented in forward direction (photograph on the top configuration was taken before photograph shown on the bottom) or vice versa. Children and adults showed sensitivity to temporal distance between events based on behavior (in some instances accuracy was higher for long compared to short temporal distance) and ERP (differential neural processing for short and long temporal distance conditions). Only adults showed sensitivity to the memory asymmetry manipulation, and only when the events occurred within a short temporal distance. A larger study is needed to confirm the present "proof of concept" study results. There is strong potential of this photo paradigm approach, combining naturalistic events with ERP, in future developmental studies, and would further our understanding of how memory behavior and the neural processes underlying memory operate in the "real world."

From vision to memory: How scene-sensitive regions support episodic memory formation during child development.

Previous brain imaging studies have identified three brain regions that selectively respond to visual scenes, the parahippocampal place area (PPA), the occipital place area (OPA), and the retrosplenial cortex (RSC). There is growing evidence that these visual scene-sensitive regions process different types of scene information and may have different developmental timelines in supporting scene perception. How these scene-sensitive regions support memory functions during child development is largely unknown. We investigated PPA, OPA and RSC activations associated with episodic memory formation in childhood (5-7 years of age) and young adulthood, using a subsequent scene memory paradigm and a functional localizer for scenes. PPA, OPA, and RSC subsequent memory activation and functional connectivity differed between children and adults. Subsequent memory effects were found in activations of all three scene regions in adults. In children, however, robust subsequent memory effects were only found in the PPA. Functional connectivity during successful encoding was significant among the three regions in adults, but not in children. PPA subsequently memory activations and PPA-RSC subsequent memory functional connectivity correlated with accuracy in adults, but not children. These age-related differences add new evidence linking protracted development of the scene-sensitive regions to the protracted development of episodic memory.

Fluctuations in Sustained Attention Explain Moment-to-Moment Shifts in Children's Memory Formation.

Why do children's memories often differ from adults' after the same experience? Whereas prior work has focused on children's immature memory mechanisms to answer this question, here we focus on the costs of attentional lapses for learning. We track sustained attention and memory formation across time in 7- to 10-year-old children and adults (n = 120) to show that sustained attention causally shapes the fate of children's individual memories. Moreover, children's attention lapsed twice as frequently as adults', and attention fluctuated with memory formation more closely in children than adults. In addition, although attentional lapses impaired memory for expected events in both children and adults, they impaired memory for unexpected events in children only. Our work reveals that sustained attention is an important cognitive factor that controls access to children's long-term memory stores. Our work also raises the possibility that developmental differences in cognitive performance stem from developmental shifts in the ability to sustain attention.

The Influence of Memory on Visual Perception in Infants, Children, and Adults.

Perception is not an independent, in-the-moment event. Instead, perceiving involves integrating prior expectations with current observations. How does this ability develop from infancy through adulthood? We examined how prior visual experience shapes visual perception in infants, children, and adults. Using an identical task across age groups, we exposed participants to pairs of colorful stimuli and implicitly measured their ability to discriminate relative saturation levels. Results showed that adult participants were biased by previously experienced exemplars, and exhibited weakened in-the-moment discrimination between different levels of saturation. In contrast, infants and children showed less influence of memory in their perception, and they actually outperformed adults in discriminating between current levels of saturation. Our findings suggest that as humans develop, their perception relies more on prior experience and less on current observation.

Does Equine Interaction Facilitate Emotional Safety and Learning for College Students within an Agricultural-Based Classroom?

Effective teaching requires an educational environment that promotes learning, and yet, developing such an environment can be challenging within today's agricultural-based classroom for educators due to the trend to a more virtual teaching format and less hands-on learning. Animal interaction, particularly equine activities, has been shown to assist educators in the development of an emotionally safe environment for promoting learning. However, research is lacking as to whether the interaction with the animal needs to be direct or indirect within the collegiate educational environment to observe benefits. Therefore, the objective of this study was to determine the impact of equine interaction, both direct and indirect, within an educational environment on the emotional safety and learning for the college student within the agricultural-based classroom. Three course types were observed within the agricultural-based educational environment that included courses with no equine interaction (Group A) and courses with equine interaction, both direct (Group B) and indirect (Group C) interaction with the horse. Indirect interaction included items such as observation of equine handling via a video or gaining knowledge from reading online materials, but not engaging in direct, hands-on activities with the horse. Development of emotional safety within the students enrolled within these courses was measured using a self-reporting emotional safety evaluation. Due to the structure of the scale, a decrease in emotional safety indicated a positive change. Learning, both development of semantic and procedural memory, was measured using a student-completed knowledge examination and an instructor-completed skill evaluation, respectively. While significant improvement in emotional safety was not observed within any of the course types, a weak negative correlation was found between emotional safety and semantic memory for students enrolled in equine courses, both direct (R = -0.55, R2 = 0.28) and indirect (R = -0.25, R2 = 0.06) interaction, finding as emotional safety scores lowered to the ideal range that knowledge improved. In addition, students within equine courses showed semantic memory development in specific areas of equine sciences (Group B: Grooming/Tacking, p = 0.03; Group C: Equine Behavior, p = 0.04) and direct equine interaction resulted in development of equine-based procedural memory in all four skill areas measured within the study (p = 0.00). As such, learning is promoted through equine interaction, whether direct or indirect interaction, within the agricultural-based classroom, suggesting that both forms of equine interaction can be a valuable educational tool for the instructor within the collegiate setting.

Neurophysiological mechanisms of cognition in the developing brain: Insights from intracranial EEG studies.

The quest to understand how the development of the brain supports the development of complex cognitive functions is fueled by advances in cognitive neuroscience methods. Intracranial EEG (iEEG) recorded directly from the developing human brain provides unprecedented spatial and temporal resolution for mapping the neurophysiological mechanisms supporting cognitive development. In this paper, we focus on episodic memory, the ability to remember detailed information about past experiences, which improves from childhood into adulthood. We review memory effects based on broadband spectral power and emphasize the importance of isolating narrowband oscillations from broadband activity to determine mechanisms of neural coordination within and between brain regions. We then review evidence of developmental variability in neural oscillations and present emerging evidence linking the development of neural oscillations to the development of memory. We conclude by proposing that the development of oscillations increases the precision of neural coordination and may be an essential factor underlying memory development. More broadly, we demonstrate how recording neural activity directly from the developing brain holds immense potential to advance our understanding of cognitive development.

Extended trajectory of spatial memory errors in typical and atypical development: The role of binding and precision.

Spatial reconstruction, a method for evaluating how individuals remember the placement of objects, has traditionally been evaluated through the aggregate estimation of placement errors. However, this approach may obscure the nature of task errors. Specifically, recent data has suggested the importance of examining the precision of responses, as well as absolute performance on item-context bindings. In contrast to traditional analysis approaches based on the distance between the target and the reconstructed item, in this study we further explored three types of errors (swap error, global error, and local distance) that may all contribute to the distance, with particular emphasis on swap errors and local distance due to their associations with item-context bindings and memory precision, respectively. We examined these errors in children aged 3-18 years, making comparisons between children with typical development (TD) and children with Down syndrome (DS), a population with known memory challenges. As expected, older children outperformed younger children in terms of overall memory accuracy. Of importance is that we measured uneven maturational trajectories of memory abilities across the various error types. Specifically, both remembered locations (irrespective of object identity) and swap errors (object-location binding errors) align with the overall memory accuracy. Memory precision, as measured by local distance in simpler set size 2 trials, mirrored overall memory accuracy. However, for more complex set size 3 trials, local distance remained stable before age 8 and showed age-related change thereafter. The group with DS showed reduced precision compared to a TD matched group, and measures of precision, and to a lesser extent binding errors, correlated with standard neuropsychological outcomes. Overall, our study contributed to a fine-grained understanding of developing spatial memory ability in a large sample of typical developing children and a memory impaired population. These findings contribute to a growing body of research examining precision as a key factor in memory performance.

Can 18-Month-Olds Revise Attributed Beliefs?

Successful social interactions rely on flexibly tracking and revising others' beliefs. These can be revised prospectively, new events leading to new beliefs, or retrospectively, when realizing that an attribution may have been incorrect. However, whether infants are capable of such belief revisions is an open question. We tested whether 18-month-olds can revise an attributed FB into a TB when they learn that a person may have witnessed an event that they initially thought she could not see. Infants first observed Experimenter 1 (E1) hiding two objects into two boxes. Then E1 left the room, and the locations of the objects were swapped. Infants then accompanied Experimenter 2 (E2) to the adjacent room. In the FB-revised-to-TB condition, infants observed E1 peeking into the experimental room through a one-way mirror, whereas in the FB-stays-FB condition, they observed E1 reading a book. After returning to the experimental room E1 requested an object by pointing to one of the boxes. In the FB-stays-FB condition, most infants chose the non-referred box, congruently with the agent's FB. However, in the FB-revised-to-TB condition, most infants chose the other, referred box. Thus, 18-month-olds revised an already attributed FB after receiving evidence that this attribution might have been wrong.

Prolonged development of forced-choice recognition when targets are paired with non-corresponding lures.

Previous research suggests that mnemonic discrimination (i.e., the ability to discriminate between previously encountered and novel stimuli even when they are highly similar) improves substantially during childhood. To further understand the development of mnemonic discrimination during childhood, the current study had 4-year-old children, 6-year-old children, and young adults complete the forced-choice Mnemonic Similarity Task (MST). The forced-choice MST offers a significant advantage in the context of developmental research because it is not sensitive to age-related differences in response criteria and includes three test formats that are theorized to be supported by different cognitive processes. A target (i.e., a previously encountered item) is paired with either a novel item (A-X), a corresponding lure (A-A'; i.e., an item mnemonically similar to the target), or a non-corresponding lure (A-B'; i.e., an item mnemonically similar to a different previously encoded item). We observed that 4-year-olds performed more poorly than 6-year-olds on the A-X and A-A' test formats, whereas both 4- and 6-year-olds performed more poorly than young adults on the A-B' test format. The MINERVA 2.2 computational model effectively accounted for these age-related differences. The model suggested that 4-year-olds have a lower learning rate (i.e., probability of encoding stimulus features) than 6-year-olds and young adults and that both 4- and 6-year-olds have greater encoding variability than young adults. These findings provide new insight into possible mechanisms underlying memory development during childhood and serve as the basis for multiple avenues of future research.

Setting boundaries: Development of neural and behavioral event cognition in early childhood.

The ongoing stream of sensory experience is so complex and ever-changing that we tend to parse this experience at "event boundaries," which structures and strengthens memory. Memory processes undergo profound change across early childhood. Whether young children also divide their ongoing processing along event boundaries, and if those boundaries relate to memory, could provide important insight into the development of memory systems. In Study 1, 4-7-year-old children and adults segmented a cartoon, and we tested their memory. Children's event boundaries were more variable than adults' and differed in location and consistency of agreement. Older children's event segmentation was more adult-like than younger children's, and children who segmented events more like adults had better memory for those events. In Study 2, we asked whether these developmental differences in event segmentation had their roots in distinct neural representations. A separate group of 4-8-year-old children watched the same cartoon while undergoing an fMRI scan. In the right hippocampus, greater pattern dissimilarity across event boundaries compared to within events was evident for both child and adult behavioral boundaries, suggesting children and adults share similar event cognition. However, the boundaries identified by a data-driven Hidden Markov Model found that a different brain region-the left and right angular gyrus-aligned only with event boundaries defined by children. Overall, these data suggest that children's event cognition is reasonably well-developed by age 4 but continues to become more adult-like across early childhood. RESEARCH HIGHLIGHTS: Adults naturally break their experience into events, which structures and strengthens memory, but less is known about children's event perception and memory. Study 1 had adults and children segment and remember events from an animated show, and Study 2 compared those segmentations to other children's fMRI data. Children show better recognition and temporal order memory and more adult-like event segmentation with age, and children who segment more like adults have better memory. Children's and adults' behavioral boundaries mapped onto pattern similarity differences in hippocampus, and children's behavioral boundaries matched a data-driven model's boundaries in angular gyrus.

Children's memory "in the wild": examining the temporal organization of free recall from a week-long camp at a local zoo.

Free-recall paradigms have greatly influenced our understanding of memory. The majority of this research involves laboratory-based events (e.g., word lists) that are studied and tested within minutes. This literature shows that adults recall events in a temporally organized way, with successive responses often coming from neighboring list positions (i.e., temporal clustering) and with enhanced memorability of items from the end of a list (i.e., recency). Temporal clustering effects are so robust that temporal organization is described as a fundamental memory property. Yet relatively little is known about the development of this temporal structure across childhood, and even less about children's memory search for real-world events occurring over an extended period. In the present work, children (N = 144; 3 age groups: 4-5-year-olds, 6-7-year-olds, 8-10-year-olds) took part in a 5-day summer camp at a local zoo. The camp involved various dynamic events, including daily animal exhibit visits. On day 5, children were asked to recall all the animals they visited. We found that overall recall performance, in terms of number of animals recalled, improved steadily across childhood. Temporal organization and recency effects showed different developmental patterns. Temporal clustering was evident in the response sequences for all age groups and became progressively stronger across childhood. In contrast, the recency advantage, when characterized as a proportion of total responses, was stable across age groups. Thus, recall dynamics in early childhood parallel that seen in adulthood, with continued development of temporal organization across middle to late childhood.

Sources of Interference in Memory Across Development.

Episodic memory involves remembering not only what happened but also where and when the event happened. This multicomponent nature introduces different sources of interference that stem from previous experience. However, it is unclear how the contributions of these sources change across development and what might cause the changes. To address these questions, we tested 4- to 5-year-olds (n = 103), 7- to 8-year-olds (n = 82), and adults (n = 70) using item- and source-recognition memory tasks with various manipulations (i.e., list length, list strength, word frequency), and we decomposed sources of interference using a computational model. We found that interference stemming from other items on the study list rapidly decreased with development, whereas interference from preexperimental contexts gradually decreased but remained the major source of interference. The model further quantified these changes, indicating that the ability to discriminate items undergoes rapid development, whereas the ability to discriminate contexts undergoes protracted development. These results elucidate fundamental aspects of memory development.

Maturity of white matter tracts is associated with episodic memory recall during development.

The structure-function relationship between white matter microstructure and episodic memory (EM) has been poorly studied in the developing brain, particularly in early childhood. Previous studies in adolescents and adults have shown that episodic memory recall is associated with prefrontal-limbic white matter microstructure. It is unknown whether this association is also observed during early ontogeny. Here, we investigated the association between prefrontal-limbic tract microstructure and EM performance in a cross-sectional sample of children aged 4 to 12 years. We used a multivariate partial least squares correlation approach to extract tract-specific latent variables representing shared information between age and diffusion parameters describing tract microstructure. Individual projections onto these latent variables describe patterns of interindividual differences in tract maturation that can be interpreted as scores of white matter tract microstructural maturity. Using these estimates of microstructural maturity, we showed that maturity scores of the uncinate fasciculus and dorsal cingulum bundle correlated with distinct measures of EM recall. Furthermore, the association between tract maturity scores and EM recall was comparable between younger and older children. Our results provide new evidence on the relation between white matter maturity and EM performance during development.

Working memory development: A 50-year assessment of research and underlying theories.

The author has thought about working memory, not always by that name, since 1969 and has conducted research on its infant and child development since the same year that the seminal work of Baddeley and Hitch (1974) was published. The present article assesses how the field of working memory development has been influenced since those years by major theoretical perspectives: empiricism (along with behaviorism), nativism (along with modularity), cognitivism (along with constructivism), and dynamic systems theory. The field has not fully discussed the point that these theoretical perspectives have helped to shape different kinds of proposed working memory systems, which in turn have deeply influenced what is researched and how it is researched. Here I discuss that mapping of theoretical viewpoints onto assumptions about working memory and trace the influence of this mapping on the field of working memory development. I illustrate where these influences have led in my own developmental research program over the years.

The fornix supports episodic memory during childhood.

Episodic memory relies on the coordination of widespread brain regions that reconstruct spatiotemporal details of an episode. These topologically dispersed brain regions can rapidly communicate through structural pathways. Research in animal and human lesion studies implicate the fornix-the major output pathway of the hippocampus-in supporting various aspects of episodic memory. Because episodic memory undergoes marked changes in early childhood, we tested the link between the fornix and episodic memory in an age window of robust memory development (ages 4-8 years). Children were tested on the stories subtest from the Children's Memory Scale, a temporal order memory task, and a source memory task. Fornix streamlines were reconstructed using probabilistic tractography to estimate fornix microstructure. In addition, we measured fornix macrostructure and computed free water. To assess selectivity of our findings, we also reconstructed the uncinate fasciculus. Findings show that children's memory increases from ages 4 to 8 and that fornix micro- and macrostructure increases between ages 4 and 8. Children's memory performance across nearly every memory task correlated with individual differences in fornix, but not uncinate fasciculus, white matter. These findings suggest that the fornix plays an important role in supporting the development of episodic memory, and potentially semantic memory, in early childhood.

Contextual features in the developing hippocampus: A representational similarity analysis.

Functional divisions of labor in support of memory have been reported along the anterior-posterior axis of the hippocampus. However, little is known about how the developing hippocampus represents associative memories along this axis. The present research employed representational similarity analysis to ask whether developmental differences exist in the extent to which the anterior versus the posterior hippocampus represent features of the context and associative memories. Functional magnetic resonance imaging data were collected during the retrieval phase of an associative recognition task from 8-year-olds, 10-year-olds, and adults (N = 58). Participants were asked to retrieve pairs of items, which were presented either in the same location as during encoding or in a flipped location. In the anterior hippocampus and only for adults, pattern similarity between the two studied pair conditions was greater than pattern similarity between studied pairs presented in the same location and novel pairs. In contrast, this difference was not significant in the posterior hippocampus. Older, but not younger, children showed a similar, albeit attenuated, similarity pattern to that of adults, but measures of patterns similarity predicted associative recognition across ages. In addition, exploratory analyses showed that similarity patterns in the adult posterior, but not anterior, hippocampus tracked the order of the runs. Overall, the results suggest functional and developmental dissociations in processing different contextual features, with the anterior hippocampus responding to salient and rapid-changing features and the posterior hippocampus responding to slower-changing features of the context.

Predicting explicit memory for meaningful cartoons from visual paired comparison in infants and toddlers.

We tested the memory of 18-, 33-, and 39-month-olds (N = 120) for dynamic stimulus material (simple cartoons) after 6 months in a visual paired comparison (VPC) task. We also tested the explicit recognition memory (ERM) for the same material. Only the oldest age group (39-month-olds) showed a significant visual (familiarity) preference at the test. Similarly, only the oldest group reliably chose the correct cartoon in the ERM test. Data from the VPC and ERM tasks did not correlate in any age group. However, we suggested a novel score (coined ΔVPC) measuring how much visual preference changes during the test phase in the VPC task. We found that this ΔVPC score (and vocabulary) predicted children's performance in the ERM task, whereas other potential predictors such as age and conventional novelty preference did not. We discuss the impact of these findings in relation to the development of implicit and explicit memory. Furthermore, we propose that VPC measures are associated with explicit memory only when the participants processed the stimuli conceptually. In such cases, we suggest that the ΔVPC score is an approximation of how demanding it is to construct the mental representation of the familiar stimulus during the test phase.

Differences in executive abilities rather than associative processes contribute to memory development.

Children's learning capabilities change while growing up. One framework that describes the cognitive and neural development of children's growing learning abilities is the two-component model. It distinguishes processes that integrate separate features into a coherent memory representation (associative component) and executive abilities, such as elaboration, evaluation, and monitoring, that support memory processing (strategic component). In an fMRI study using an object-location association paradigm, we investigated how the two components influence memory performance across development. We tested children (10-12 years, n = 31), late adolescents (18 years, n = 29), and adults (25+ years, n = 30). For studying the associative component, we also probed how the utilisation of prior knowledge (schemas) facilitates memory across age groups. Children had overall lower retrieval performance, while adolescents and adults did not differ from each other. All groups benefitted from schemas, but this effect did not differ between groups. Performance differences between groups were associated with deactivation of the dorsal medial prefrontal cortex (dmPFC), which in turn was linked to executive functioning. These patterns were stronger in adolescents and adults and seemed absent in children. Thus, the children's executive system, the strategic component, is not as mature and thus cannot facilitate memory performance in the same way as in adolescents/adults. In contrast, we did not find age-related differences in the associative component; with activity in the angular gyrus predicting memory performance systematically across groups. Overall, our results suggest that differences of executive rather than associative abilities explain memory differences between children, adolescents, and adults.