Age differences in generalization, memory specificity, and their overnight fate in childhood.

Memory enables generalization to new situations, and memory specificity that preserves individual episodes. This study investigated generalization, memory specificity, and their overnight fate in 141 4- to 8-year-olds (computerized memory game; 71 females, tested 2020-2021 in Germany). The results replicated age effects in generalization and memory specificity, and a contingency of generalization on object conceptual properties and interobject semantic proximity. Age effects were stronger in generalization than in memory specificity, and generalization was more closely linked to the explicit regularity knowledge in older than in younger children. After an overnight delay, older children retained more generalized and specific memories and showed greater gains but only in generalization. These findings reveal distinct age differences in generalization and memory specificity across childhood.

Children show adult-like hippocampal pattern similarity for familiar but not novel events.

The ability to detect differences among similar events in our lives is a crucial aspect of successful episodic memory performance, which develops across early childhood. The neural substrate of this ability is supported by operations in the medial temporal lobe (MTL). Here, we used representational similarity analysis (RSA) to measure neural pattern similarity in hippocampus, perirhinal cortex, and parahippocampal cortex for 4- to 10-year-old children and adults during naturalistic viewing of clips from the same compared to different movies. Further, we assessed the role of prior exposure to individual movie clips on pattern similarity in the MTL. In both age groups, neural pattern similarity in hippocampus was lower for clips drawn from the same movies compared to those drawn from different movies, suggesting that related content activates processes focused on keeping representations with shared content distinct. However, children showed this only for movies with which they had prior exposures, whereas adults showed the effect regardless of any prior exposures to the movies. These findings suggest that children require repeated exposure to stimuli to show adult-like MTL functioning in distinguishing among similar events.

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.

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.

Contingency of semantic generalization on episodic specificity varies across development.

Semantic memory-general knowledge of ideas and concepts-includes generalization processes that support inference. Episodic memory, on the other hand, preserves the specificity of individual events by binding together unique combinations of elements from an episode and relies on pattern separation to distinguish similar experiences. These two memory systems play complementary roles, supporting different mnemonic goals, but the nature and extent of their interdependence is unclear.1,2 Some models suggest that new information is encoded initially as hippocampus-dependent episodic memory and then, either through repetition or gist extraction, becomes semantic over time.3,4 These models also posit a neocortical route to semantic memory acquisition exists that can bypass the hippocampus.3 Both proposed routes are slow learning mechanisms, yet generalization can occur rapidly. Recent models suggest that fast generalization relies, in part, on the retrieval of individual but related episodes.5,6 Such episodic memory gating mechanisms render fast generalization contingent on the memory specificity of instances, a pattern that has been observed in adults.7,8 None of these models take into account the observation that generalization and episodic specificity have asynchronous developmental profiles, with generalization emerging years before episodic memory.9,10 We ask two questions about generalized and specific memory during early childhood: first, is rapid generalization contingent on remembering specific past memories? And second, does the strength or nature of this contingency differ across development? We found that the interdependence of generalization and episodic memory varies across development: generalization success in adults, but not in children, was contingent on context binding.

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.

Dissecting the Fornix in Basic Memory Processes and Neuropsychiatric Disease: A Review.

Background: The fornix is the primary axonal tract of the hippocampus, connecting it to modulatory subcortical structures. This review reveals that fornix damage causes cognitive deficits that closely mirror those resulting from hippocampal lesions. Methods: We reviewed the literature on the fornix, spanning non-human animal lesion research, clinical case studies of human patients with fornix damage, as well as diffusion-weighted imaging (DWI) work that evaluates fornix microstructure in vivo. Results: The fornix is essential for memory formation because it serves as the conduit for theta rhythms and acetylcholine, as well as providing mnemonic representations to deep brain structures that guide motivated behavior, such as when and where to eat. In rodents and non-human primates, fornix lesions lead to deficits in conditioning, reversal learning, and navigation. In humans, damage to the fornix manifests as anterograde amnesia. DWI research reveals that the fornix plays a key role in mild cognitive impairment and Alzheimer's Disease, and can potentially predict conversion from the former to the latter. Emerging DWI findings link perturbations in this structure to schizophrenia, mood disorders, and eating disorders. Cutting-edge research has investigated how deep brain stimulation of the fornix can potentially attenuate memory loss, control epileptic seizures, and even improve mood. Conclusions: The fornix is essential to a fully functioning memory system and is implicated in nearly all neurological functions that rely on the hippocampus. Future research needs to use optimized DWI methods to study the fornix in vivo, which we discuss, given the difficult nature of fornix reconstruction. Impact Statement The fornix is a white matter tract that connects the hippocampus to several subcortical brain regions and is pivotal for episodic memory functioning. Functionally, the fornix transmits essential neurotransmitters, as well as theta rhythms, to the hippocampus. In addition, it is the conduit by which memories guide decisions. The fornix is biomedically important because lesions to this tract result in irreversible anterograde amnesia. Research using in vivo imaging methods has linked fornix pathology to cognitive aging, mild cognitive impairment, psychosis, epilepsy, and, importantly, Alzheimer's Disease.

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.

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.

Building up and wearing down episodic memory: Mnemonic discrimination and relational binding.

Our capacity to form and retrieve episodic memories improves over childhood but declines in old age. Understanding these changes requires decomposing episodic memory into its components. Two such components are (a) mnemonic discrimination of similar people, objects, and contexts, and (b) relational binding of these elements. We designed novel memory tasks to assess these component processes using animations that are appropriate across the life span (ages 4-80 in our sample). In Experiment 1, we assessed mnemonic discrimination of objects as well as relational binding, in a common task format. Both components follow an inverted U-shaped curve across age but were positively correlated only in the aging group. In Experiment 2, we examined mnemonic discrimination of context and its effect on relational binding. Relational memory in low-similarity contexts showed robust gains between the ages of 4 and 6, whereas 6-year-olds performed similarly to adults. In contrast, relational memory in high-similarity contexts showed more protracted development, with 4- and 6-year-olds both performing worse than young adults and not differing from each other. Relational memory in both context conditions declined in aging. This multiprocess approach provides important theoretical insights into life span changes in episodic memory. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Hippocampal signatures of awake targeted memory reactivation.

Dominant theories of episodic memory propose that a key mechanism of memory consolidation is replay-a process, whereby neural patterns of activation during learning are reinstated during offline post-learning periods. Here, we tested whether key signatures of replay defined by studies in rodents, such as recapitulation of specific memory traces, as well as sequences, are apparent in humans during post-encoding memory reactivation. Thirty participants underwent functional imaging that consisted of interleaved encoding and rest periods. During an offline period of wakeful rest, we biased reactivation towards some memories by presenting sound cues that had previously been associated with particular stimulus sequences. Results showed that targeted hippocampal reactivation was biased towards cued memory sequences and that reactivation signatures preserved the temporal order of particular sequences. Importantly, the biased reactivation was related to differences in subsequent memory, suggesting that preferential reactivation may be a mechanism by which specific memory traces can be strengthened for enhanced subsequent memory retrieval.

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.

Hippocampal Maturation Drives Memory from Generalization to Specificity.

During early ontogeny, the rapid and cumulative acquisition of world knowledge contrasts with slower improvements in the ability to lay down detailed and long-lasting episodic memories. This emphasis on generalization at the expense of specificity persists well into middle childhood and possibly into adolescence. During this period, recognizing regularities, forming stable representations of recurring episodes, predicting the structure of future events, and building up semantic knowledge may be prioritized over remembering specific episodes. We highlight recent behavioral and neuroimaging evidence suggesting that maturational differences among subfields within the hippocampus contribute to the developmental lead-lag relation between generalization and specificity, and lay out future research directions.

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.

Familiarity influences on direct and indirect associative memory for objects in scenes.

Remembering arbitrary associations, such as unrelated word pairs or object-background pairs, appears to depend on recollection. However, for cases in which the components of an association share pre-existing semantic relations, can familiarity support associative recognition? In two experiments with congruent object-background pairings, we found that participants were successful at direct and indirect associative recognition in both 1000 ms time restriction (speeded) and unlimited response time (non-speeded) test conditions. Because dual-process theory postulates that familiarity is less impacted by speeded responses, relative to recollection, these findings suggest that congruent object-background associations may not necessitate recollection when an arbitrary link is not constructed at encoding. Experiment 3 compared direct associative memory for congruent and incongruent object-background pairs in speeded and non-speeded test conditions. We found that participants in the non-speeded condition performed comparably with congruent and incongruent pairs, whereas those in the speeded condition performed significantly worse on the incongruent pairs than on the congruent pairs. Together, these findings suggest a differential role of familiarity and recollection depending on the types of associations. Implications for dual-process recognition memory models and levels of unitization framework are discussed.

White matter structural connectivity and episodic memory in early childhood.

Episodic memory undergoes dramatic improvement in early childhood; the reason for this is poorly understood. In adults, episodic memory relies on a distributed neural network. Key brain regions that supporting these processes include the hippocampus, portions of the parietal cortex, and portions of prefrontal cortex, each of which shows different developmental profiles. Here we asked whether developmental differences in the axonal pathways connecting these regions may account for the robust gains in episodic memory in young children. Using diffusion weighted imaging, we examined whether white matter connectivity between brain regions implicated in episodic memory differed with age, and were associated with memory performance differences in 4- and 6-year-old children. Results revealed that white matter connecting the hippocampus to the inferior parietal lobule significantly predicted children's performance on episodic memory tasks. In contrast, variation in the white matter connecting the hippocampus to the medial prefrontal cortex did not relate to memory performance. These findings suggest that structural connectivity between the hippocampus and lateral parietal regions is relevant to the development of episodic memory.

Never forget a name: white matter connectivity predicts person memory.

Through learning and practice, we can acquire numerous skills, ranging from the simple (whistling) to the complex (memorizing operettas in a foreign language). It has been proposed that complex learning requires a network of brain regions that interact with one another via white matter pathways. One candidate white matter pathway, the uncinate fasciculus (UF), has exhibited mixed results for this hypothesis: some studies have shown UF involvement across a range of memory tasks, while other studies report null results. Here, we tested the hypothesis that the UF supports associative memory processes and that this tract can be parcellated into sub-tracts that support specific types of memory. Healthy young adults performed behavioral tasks (two face-name learning tasks, one word pair memory task) and underwent a diffusion-weighted imaging scan. Our results revealed that variation in UF microstructure was significantly associated with individual differences in performance on both face-name tasks, as well as the word association memory task. A UF sub-tract, functionally defined by its connectivity between face-selective regions in the anterior temporal lobe and orbitofrontal cortex, selectively predicted face-name learning. In contrast, connectivity between the fusiform face patch and both anterior face patches had no predictive validity. These findings suggest that there is a robust and replicable relationship between the UF and associative learning and memory. Moreover, this large white matter pathway can be subdivided to reveal discrete functional profiles.

The relation between navigation strategy and associative memory: An individual differences approach.

Although the hippocampus is implicated in both spatial navigation and associative memory, very little is known about whether individual differences in the 2 domains covary. People who prefer to navigate using a hippocampal-dependent place strategy may show better performance on associative memory tasks than those who prefer a caudate-dependent response strategy (Bohbot, Gupta, Banner, & Dahmani, 2011), but not all studies suggest such an effect (Woollett & Maguire, 2009, 2012). Here we tested nonexpert young adults and found that preference for a place strategy positively correlated with spatial (object-location) associative memory performance but did not correlate with nonspatial (face-name) associative memory performance. Importantly, these correlations differed from each other, indicating that the relation between navigation strategy and associative memory is specific to the spatial domain. In addition, the 2 associative memory tasks significantly correlated, suggesting that object-location memory taps into processes relevant to both hippocampal-dependent navigation and nonspatial associative memory. Our findings also suggest that individual differences in spatial associative memory may account for some of the variance in navigation strategies.

Not enough familiarity for fluency: definitional encoding increases familiarity but does not lead to fluency attribution in associative recognition.

Five experiments were conducted to test whether encoding manipulations thought to encourage unitization would affect fluency attribution in associative recognition memory. Experiments 1a and 1b, which utilized a speeded recognition memory test, demonstrated that definitional encoding increased reliance on familiarity during the recognition memory test. Experiments 2a, 2b, and 3, however, replicated previous research that had shown that fluency is unlikely to be attributed as evidence of previous occurrence in associative recognition (Westerman, Journal of Experimental Psychology: Learning, Memory, and Cognition 27:723-732, 2001). The results put limits on the degree to which fluency can influence recognition memory judgments, even in cases of enhanced familiarity, and are consistent with previous work suggesting that participants have preexperimental expectations about fluency that are difficult to change (e.g., Miller, Lloyd, & Westerman, Journal of Memory and Language 58:1080-1094, 2008), as well as with work suggesting that fluency has less of an influence on recognition memory decisions that are conceptual in nature (Parks, Journal of Experimental Psychology: Learning, Memory, and Cognition 39:1280-1286, 2013).