Children's Memory for Events: The Challenge of Free Recall.

Early childhood is a critical period for episodic memory development, with sharp behavioral improvements between ages 4 to 7 years. Prior work has demonstrated this extensively with prompted memory tasks, but we explored performance on unprompted, free recall of a naturalistic experience in children, and how their performance relates to other cognitive measures. We asked children and adults to view a television episode, a naturalistic task for which there exists a ground truth, and assessed their free recall memory for the episode. Children's free recall performance improved dramatically with age, with many young children producing no verbal free recall whatsoever, although prompted recognition memory measures showed retention of material. However, the detail in free recall was related to both recognition and temporal order forced-choice memory performance in our full sample, showing agreement among memory measures. Free recall was strongly predicted by verbal skills, suggesting that children's sparse recall reflects verbal skill development rather than a pure mnemonic deficit. We propose that free recall has a more protracted developmental trajectory because it requires more substantial verbal skills as well as metacognitive skills that direct memory search, as compared with forced-choice memory tasks.

Unpacking the navigation toolbox: insights from comparative cognition.

The study of navigation is informed by ethological data from many species, laboratory investigation at behavioural and neurobiological levels, and computational modelling. However, the data are often species-specific, making it challenging to develop general models of how biology supports behaviour. Wiener et al. outlined a framework for organizing the results across taxa, called the 'navigation toolbox' (Wiener et al. In Animal thinking: contemporary issues in comparative cognition (eds R Menzel, J Fischer), pp. 51-76). This framework proposes that spatial cognition is a hierarchical process in which sensory inputs at the lowest level are successively combined into ever-more complex representations, culminating in a metric or quasi-metric internal model of the world (cognitive map). Some animals, notably humans, also use symbolic representations to produce an external representation, such as a verbal description, signpost or map that allows communication of spatial information or instructions between individuals. Recently, new discoveries have extended our understanding of how spatial representations are constructed, highlighting that the hierarchical relationships are bidirectional, with higher levels feeding back to influence lower levels. In the light of these new developments, we revisit the navigation toolbox, elaborate it and incorporate new findings. The toolbox provides a common framework within which the results from different taxa can be described and compared, yielding a more detailed, mechanistic and generalized understanding of navigation.

What have we learned from research on the "geometric module"?

This article is an overview of the research and controversy initiated by Cheng's (Cognition, 23(2), 149-178, 1986) article hypothesizing a purely geometric module in spatial representation. Hundreds of experiments later, we know much more about spatial behavior across a very wide array of species, ages, and kinds of conditions, but there is still no consensus model of the phenomena. I argue for an adaptive combination approach that entails several principles: (1) a focus on ecological niches and the spatial information they offer; (2) an approach to development that is experience-expectant: (3) continued plasticity as environmental conditions change; (4) language as one of many cognitive tools that can support spatial behavior.

Tracing the origins of the STEM gender gap: The contribution of childhood spatial skills.

Despite some gains, women continue to be underrepresented in many science, technology, engineering, and math (STEM) fields. Using a national longitudinal dataset of 690 participants born in 1991, we tested whether spatial skills, measured in middle childhood, would help explain this gender gap. We modeled the relation between 4th-grade spatial skills and STEM majors while simultaneously accounting for competing cognitive and motivational mechanisms. Strong spatial skills in 4th grade directly increased the likelihood of choosing STEM college majors, above and beyond math achievement and motivation, verbal achievement and motivation, and family background. Additionally, 4th-grade spatial skills indirectly predicted STEM major choice via math achievement and motivation in the intervening years. Further, our findings suggest that gender differences in 4th-grade spatial skills contribute to women's underrepresentation in STEM majors. RESEARCH HIGHLIGHTS: Using a national longitudinal dataset, we found 4th-grade spatial skills directly predicted STEM college major choice after accounting for multiple cognitive and motivational mechanisms. Strong spatial skills in 4th grade also elevated STEM major choice via enhanced math achievement and motivation in the intervening years. Gender differences in 4th-grade spatial skills contributed to women's underrepresentation in STEM college majors.

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.

The Ontogeny of Hippocampus-Dependent Memories.

The formation of memories that contain information about the specific time and place of acquisition, which are commonly referred to as "autobiographical" or "episodic" memories, critically relies on the hippocampus and on a series of interconnected structures located in the medial temporal lobe of the mammalian brain. The observation that adults retain very few of these memories from the first years of their life has fueled a long-standing debate on whether infants can make the types of memories that in adults are processed by the hippocampus-dependent memory system, and whether the hippocampus is involved in learning and memory processes early in life. Recent evidence shows that, even at a time when its circuitry is not yet mature, the infant hippocampus is able to produce long-lasting memories. However, the ability to acquire and store such memories relies on molecular pathways and network-based activity dynamics different from the adult system, which mature with age. The mechanisms underlying the formation of hippocampus-dependent memories during infancy, and the role that experience exerts in promoting the maturation of the hippocampus-dependent memory system, remain to be understood. In this review, we discuss recent advances in our understanding of the ontogeny and the biological correlates of hippocampus-dependent memories.

Longitudinal development of cognitive mapping from childhood to adolescence.

Cross-sectional studies have suggested that the ability to form cognitive maps increases throughout childhood and reaches adult levels during early adolescence. However, adults show large individual differences in their ability to relate local routes to form a global map. Children also vary, but when does variation stabilize? We asked participants from a previously published cross-sectional study [Journal of Experimental Child Psychology (2018), Vol. 170, pp. 86-106] to return for a second session of testing 3 years later to examine whether longitudinal stability is more evident at older ages. The subsample of 50 of the original 105 participants available for retesting did not differ from the original sample on male-female ratio or Session 1 task performance. We reassessed performance on the Virtual Silcton navigation paradigm, the Spatial Orientation Test (SOT), and the Mental Rotation Test (MRT) and added parents' scores on the SOT and MRT at Timepoint 2. Our initial analyses of normative development aligned with prior cross-sectional findings; overall navigation performance reached adult levels of proficiency around 12 years of age. In addition, variation in route integration abilities, as measured by between-route pointing, stabilized around 12 years of age; that is, longitudinal stability was higher in the older cohort than in the younger cohort. The same pattern appeared for the MRT.

Understanding relational binding in early childhood: Interacting effects of overlap and delay.

Episodic memories typically share overlapping elements in distinctive combinations, and to be valuable for future behavior they need to withstand delays. There is relatively little work on whether children have special difficulty with overlap or withstanding delay. However, Yim, Dennis, and Sloutsky (Psychological Science, 2013, Vol. 24, pp. 2163-2172) suggested that extensive overlap is more problematic for younger children, and Darby and Sloutsky (Psychological Science, 2015, Vol. 26, pp. 1937-1946) reported that a 48-h delay period actually improves children's memory for overlapping pairs of items. In the current study, we asked how children's episodic memory is affected by stimulus overlap, delay, and age using visual stimuli containing either overlapping or unique item pairs. Children aged 4 and 6 years were tested both immediately and after a 24-h delay. As expected, older children performed better than younger children, and both age groups performed worse on overlapping pairs. Surprisingly, the 24-h delay had only a marginal effect on overall accuracy. Although there were no interactions, when errors were examined, there was evidence that delay buffered memory for overlapping pairs against cross-contextual confusion for younger children.

Pattern separation and pattern completion: Behaviorally separable processes?

Episodic memory capacity requires several processes, including mnemonic discrimination of similar experiences, termed pattern separation, and holistic retrieval of multidimensional experiences given a cue, termed pattern completion. Both computations seem to rely on the hippocampus proper, but they also seem to be instantiated by distinct hippocampal subfields. Thus, we investigated whether individual differences in behavioral expressions of pattern separation and pattern completion were correlated after accounting for general mnemonic ability. Young adult participants learned events comprised of a scene-animal-object triad. In the pattern separation task, we estimated mnemonic discrimination using lure classification for events that contained a similar lure element. In the pattern completion task, we estimated holistic recollection using dependency in retrieval success for different associations from the same event. Although overall accuracies for the two tasks correlated as expected, specific measures of individual variation in holistic retrieval and mnemonic discrimination did not correlate, suggesting that these two processes involve distinguishable properties of episodic memory.

Relational binding and holistic retrieval in ageing.

Episodic memory binds together diverse elements of an event into a cohesive unit. This property enables the reconstruction of multidimensional experiences when triggered by a cue related to a past event via pattern completion processes. Such holistic retrieval is evident in young adults, as shown by dependency in the retrieval success for different associations from the same event [Horner, A. J., & Burgess, N. The associative structure of memory for multi-element events. Journal of Experimental Psychology: General, 142(4), 1370-1383. https://doi.org/10.1037/a0033626, 2013; Horner, A. J., & Burgess, N. (2014). Pattern completion in multielement event engrams. Current Biology, 24(9), 988-992. https://doi.org/10.1016/j.cub.2014.03.012, 2014]. Aspects of episodic memory capacity are vulnerable to ageing processes, including reduced abilities to form linkages among aspects of an event through relational binding (Naveh-Benjamin, 2000). Here, we used dependency analyses to examine whether older adults retrieve events holistically, and whether the degree of holistic retrieval declines with old age. We found that both young and older adults retrieved events as an integrated unit, but older adults showed a lower magnitude of holistic retrieval compared to young adults. Holistic retrieval declined with advancing age, even after controlling for pairwise relational binding performance. These results suggest that a decline in holistic retrieval is an aspect of episodic memory decrements in cognitive ageing.

It's All in the Details: Relations Between Young Children's Developing Pattern Separation Abilities and Hippocampal Subfield Volumes.

The ability to keep similar experiences separate in memory is critical for forming unique and lasting memories, as many events share overlapping features (e.g., birthday parties, holidays). Research on memory in young children suggests their memories often lack high-resolution details, i.e., show impoverished pattern separation (PS). Recently developed assessments of PS suitable for children allow us to relate the formation of distinct, detailed memories for the development of the hippocampus, a neural structure critical for this ability in adults. The hippocampus displays a protracted developmental profile and underlies the ability to form detailed memories. This study examined age-related differences in hippocampal subfield volumes in 4- to 8-year-old children and relations with performance on a mnemonic similarity task (MST) designed to index memory specificity. Results revealed age-moderated associations between MST performance and cornu ammonis 2-4/dentate gyrus subfields. Specifically, age-related differences in the ability to form detailed memories tracked with normative patterns of volume increases followed by reductions over this age range. That is, greater volume correlated with better performance in younger children, whereas smaller volume correlated with better performance in older children. These findings support the hypothesis that developmental differences in hippocampal circuitry contribute to age-related improvements in detailed memory formation during this period.

How many apples make a quarter? The challenge of discrete proportional formats.

Proportional judgments are easier for children in continuous formats rather than discretized ones (e.g., liquid in a beaker vs. in a beaker with unit markings). Continuous formats tap a basic sense of approximation magnitude, whereas discretized formats evoke erroneous counting strategies. On this account, truly discrete formats with separated objects should be even harder. This study (N = 565 7- to 12-year-old children) investigated that prediction. It also examined whether the format effects vary with children's fraction knowledge (FK; part-whole relations, computation, and fraction number line estimation). As found previously, discretized formats were more challenging than continuous ones; as predicted, discrete formats were yet harder. The format effect interacted with FK. Low-FK children were above chance only with continuous formats, medium-FK children struggled with discrete formats only, and high-FK children did well with all three formats.

Development of Holistic Episodic Recollection.

Episodic memory binds the diverse elements of an event into a coherent representation. This coherence allows for the reconstruction of different aspects of an experience when triggered by a cue related to a past event-a process of pattern completion. Previous work has shown that such holistic recollection is evident in young adults, as revealed by dependency in retrieval success for various associations from the same event. In addition, episodic memory shows clear quantitative increases during early childhood. However, the ontogeny of holistic recollection is uncharted. Using dependency analyses, we found here that 4-year-olds (n = 32), 6-year-olds (n = 30), and young adults (n = 31) all retrieved complex events in a holistic manner; specifically, retrieval accuracy for one aspect of an event predicted accuracy for other aspects of the same event. However, the degree of holistic retrieval increased from the age 4 to adulthood. Thus, extended refinement of multiway binding may be one aspect of episodic memory development.

Navigation and the developing brain.

As babies rapidly acquire motor skills that give them increasingly independent and wide-ranging access to the environment over the first two years of human life, they decrease their reliance on habit systems for spatial localization, switching to their emerging inertial navigation system and to allocentric frameworks. Initial place learning is evident towards the end of the period. From 3 to 10 years, children calibrate their ability to encode various sources of spatial information (inertial information, geometric cues, beacons, proximal landmarks and distal landmarks) and begin to combine cues, both within and across systems. Geometric cues are important, but do not constitute an innate and encapsulated module. In addition, from 3 to 10 years, children build the capacity to think about frames of reference different from their current one (i.e. to perform perspective taking). By around 12 years, we see adult-level performance and adult patterns of individual differences on cognitive mapping tasks requiring the integration of vista views of space into environmental space. These lines of development are continuous rather than stage-like. Spatial development builds on important beginnings in the neural systems of newborns, but changes in experience-expectant ways with motor development, action in the world and success-failure feedback. Human systems for integrating and manipulating spatial information also benefit from symbolic capacities and technological inventions.

Gain-Loss Framing Enhances Mnemonic Discrimination in Preschoolers.

Episodic memory relies on discriminating among similar elements of episodes. Mnemonic discrimination is relatively poor at age 4, and then improves markedly. We investigated whether motivation to encode items with fine-grain resolution would change this picture of development, using an engaging computer-administered memory task in which a bird ate items that made her healthier (gain frame), sicker (loss frame), or led to no change (control condition). Using gain-loss framing led to enhanced mnemonic discrimination in 4- and 5-year-olds, but did not affect older children or adults. Despite this differential improvement, age-related differences persisted. An additional finding was that loss-framing led to greater mnemonic discrimination than gain-framing across age groups. Motivation only partially accounts for the improvement in mnemonic discrimination.

The ontogeny of relational memory and pattern separation.

Episodic memory relies on memory for the relations among multiple elements of an event and the ability to discriminate among similar elements of episodes. The latter phenomenon, termed pattern separation, has been studied mainly in young and older adults with relatively little research on children. Building on prior work with young children, we created an engaging computer-administered relational memory task assessing what-where relations. We also modified the Mnemonic Similarity Task used to assess pattern discrimination in young and older adults for use with preschool children. Results showed that 4-year-olds performed significantly worse than 6-year-olds and adults on both tasks, whereas 6-year-olds and adults performed comparably, even though there were no ceiling effects. However, performance on the two tasks did not correlate, suggesting that two distinct mnemonic processes with different developmental trajectories may contribute to age-related changes in episodic memory.

Charting the development of cognitive mapping.

Developmental research beginning in the 1970s has suggested that children's ability to form cognitive maps reaches adult levels during early adolescence. However, this research has used a variety of testing procedures, often in real-world environments, which have been difficult to share widely across labs and to use to probe components of mapping, individual differences in success, and possible mechanisms of development and reasons for individual variation. In this study, we charted the development of cognitive mapping using a virtual navigation paradigm, Silcton, that allows for testing samples of substantial size in a uniform way and in which adults show marked individual differences in the formation of accurate route representations and/or in route integration. The current study tested children aged between 8 and 16 years. In terms of components of normative development, children's performance reached adult levels of proficiency at around age 12, but route representation progressed significantly more quickly than route integration. In terms of individual differences, by age 12 children could be grouped into the same three categories evident in adults: imprecise navigators (who form only imprecise ideas of routes), non-integrators (who represent routes more accurately but are imprecise in relating two routes), and integrators (who relate the two routes and, thus, form cognitive maps). Thus, individual differences likely originate during childhood. In terms of correlates, perspective-taking skills predicted navigation performance better than mental rotation skills, in accord with the view that perspective taking operates on extrinsic spatial representations, whereas mental rotation taps intrinsic spatial representations.

I. SPATIAL SKILLS, THEIR DEVELOPMENT, AND THEIR LINKS TO MATHEMATICS.

Understanding the development of spatial skills is important for promoting school readiness and improving overall success in STEM (science, technology, engineering, and mathematics) fields (e.g., Wai, Lubinski, Benbow, & Steiger, 2010). Children use their spatial skills to understand the world, including visualizing how objects fit together, and can practice them via spatial assembly activities (e.g., puzzles or blocks). These skills are incorporated into measures of overall intelligence and have been linked to success in subjects like mathematics (Mix & Cheng, 2012) and science (Pallrand & Seeber, 1984; Pribyl & Bodner, 1987). This monograph sought to answer four questions about early spatial skill development: 1) Can we reliably measure spatial skills in 3- and 4-year-olds?; 2) Do spatial skills measured at 3 predict spatial skills at age 5?; 3) Do preschool spatial skills predict mathematics skills at age 5?; and 4) What factors contribute to individual differences in preschool spatial skills (e.g., SES, gender, fine-motor skills, vocabulary, and executive function)? Longitudinal data generated from a new spatial skill test for 3-year-old children, called the TOSA (Test of Spatial Assembly), show that it is a reliable and valid measure of early spatial skills that provides strong prediction to spatial skills measured with established tests at age 5. New data using this measure finds links between early spatial skill and mathematics, language, and executive function skills. Analyses suggest that preschool spatial experiences may play a central role in children's mathematical skills around the time of school entry. Executive function skills provide an additional unique contribution to predicting mathematical performance. In addition, individual differences, specifically socioeconomic status, are related to spatial and mathematical skill. We conclude by exploring ways of providing rich early spatial experiences to children.

Commentary on Leibovich et al.: What next?

The conclusions reached by Leibovich et al. urge the field to regroup and consider new ways of conceptualizing quantitative development. We suggest three potential directions for new research that follow from the authors' extensive review, as well as building on the common ground we can take from decades of research in this area.