Examining the development of memory for temporal order and the neural substrates that support it

Episodic memory—memory for events in the context of a particular time and place—is a complex construct with a protracted development. One defining and critical feature of episodic memory is memory for temporal order, or the ability to remember the order of sequences of events (e.g., X happened before Y). Memory for temporal order is largely thought to be dependent on a neural structure in the medial temporal lobe (MTL), the hippocampus. Previous work has shown continued behavioral improvements in episodic memory in general and specifically memory for temporal order across middle to late childhood (i.e. 7-11-years-old). However, the underlying factors contributing to this development are unclear. One factor may be the structural changes in subregions along the longitudinal axis of the hippocampus that also occur during middle to late childhood. However, these behavioral and neural changes have yet to be linked during development. The present study examined, in a group of children (7-11-year-olds) and young adults, age-related differences in performance on a memory for temporal order task, age-related difference in volume along the longitudinal axis of the hippocampus using structural MRI, and the relation between memory performance and hippocampal volume. Age-related improvements were found in both the encoding and retrieval of temporal order. Manual parcellation of the hippocampus replicated previous work: adults had smaller hippocampal head and tail and larger body than children. While no relation between hippocampal subregions and retrieval of temporal order were found, some differential patterns for adults and children emerged for the relation between encoding of temporal order and hippocampal subregions

Protracted development of brain systems underlying working memory in adolescence: a longitudinal study

Working memory (WM), the ability to hold information on line to guide planned behavior, continues to improve through adolescence in parallel with brain maturational processes of systems known to support it. Initial studies have only examined individuals once or twice, limiting our understanding of developmental trajectories, leading to sparse and conflicting results. Further, it is unclear how age-related changes in WM performance and neural processes are associated, and what mechanisms might underlie these changes. In this study, we report on developmental improvements of WM performance and changes in brain function and connectivity of systems underlying WM using functional magnetic resonance imaging (fMRI) and diffusion tensor imaging (DTI), in a large longitudinal sample in which participants were followed annually for up to nine years. First, results confirmed that WM performance continues to improve into the early 20's. Alongside these refinements, brain activity in the frontal eye fields (FEF) and parietal cortex continue to change during this time; age-related changes in prefrontal regions were specifically associated with WM performance, suggesting a primary role in WM improvements. Supporting these changes, task-related functional connectivity from dorsolateral prefrontal cortex (DLPFC) to FEF, visual association cortex (VAC), and cingulate regions continued to change during adolescence and were related to WM development. Greater connectivity was associated with less mature behavior, suggesting a decreased reliance on top-down communication to support WM with development. DTI results indicated robust increases in white matter integrity across the brain with the several tracts connecting prefrontal and posterior systems, continuing to mature into early adulthood. Further, white matter measures were correlated with behavior, functional activity, and functional connectivity, suggesting that the development of structural connections may provide a scaffold on which cognitive and functional brain development can specialize. Taken together, these results suggest that while regional prefrontal function supports the transition from childhood to adolescence, the period of transition to adult level WM performance is characterized, by enhancements in prefrontal functional and structural connectivity to posterior regions supporting mnemonic aspects of working memory residing in attention and visual association regions

Hippocampal maturity promotes memory distinctiveness in childhood and adolescence

Adaptive learning systems need to meet two complementary and partially conflicting goals: detecting regularities in the world versus remembering specific events. The hippocampus (HC) keeps a fine balance between computations that extract commonalities of incoming information (i.e., pattern completion) and computations that enable encoding of highly similar events into unique representations (i.e., pattern separation). Histological evidence from young rhesus monkeys suggests that HC development is characterized by the differential development of intrahippocampal subfields and associated networks. However, due to challenges in the in vivo investigation of such developmental organization, the ontogenetic timing of HC subfield maturation remains controversial. Delineating its course is important, as it directly influences the fine balance between pattern separation and pattern completion operations and, thus, developmental changes in learning and memory. Here, we relate in vivo, high-resolution structural magnetic resonance imaging data of HC subfields to behavioral memory performance in children aged 6–14 y and in young adults. We identify a multivariate profile of age-related differences in intrahippocampal structures and show that HC maturity as captured by this pattern is associated with age differences in the differential encoding of unique memory representations

How does episodic memory develop in adolescence?

Key areas of the episodic memory (EM) network demonstrate changing structure and volume during adolescence. EM is multifaceted and yet studies of EM thus far have largely examined single components, used different methods and have unsurprisingly yielded inconsistent results. The Treasure Hunt task is a single paradigm that allows parallel investigation of memory content, associative structure, and the impact of different retrieval support. Combining the cognitive and neurobiological accounts, we hypothesized that some elements of EM performance may decline in late adolescence owing to considerable restructuring of the hippocampus at this time. Using the Treasure Hunt task, we examined EM performance in 80 participants aged 10-17 yr. Results demonstrated a cubic trajectory with youngest and oldest participants performing worst. This was emphasized in associative memory, which aligns well with existing literature indicating hippocampal restructuring in later adolescence. It is proposed that memory development may follow a nonlinear path as children approach adulthood, but that future work is required to confirm and extend the trends demonstrated in this study

The Role of Visual Association Cortex in Associative Memory Formation across Development

Associative learning underlies the formation of new episodic memories. Associative memory improves across development, and this age-related improvement is supported by the development of the hippocampus and pFC. Recent work, however, additionally suggests a role for visual association cortex in the formation of associative memories. This study investigated the role of category-preferential visual processing regions in associative memory across development using a paired associate learning task in a sample of 56 youths (age 6–19 years). Participants were asked to bind an emotional face with an object while undergoing fMRI scanning. Outside the scanner, participants completed a memory test. We first investigated age-related changes in neural recruitment and found linear age-related increases in activation in lateral occipital cortex and fusiform gyrus, which are involved in visual processing of objects and faces, respectively. Furthermore, greater activation in these visual processing regions was associated with better subsequent memory for pairs over and above the effect of age and of hippocampal and pFC activation on performance. Recruitment of these visual processing regions mediated the association between age and memory performance, over and above the effects of hippocampal activation. Taken together, these findings extend the existing literature to suggest that greater recruitment of category-preferential visual processing regions during encoding of associative memories is a neural mechanism explaining improved memory across development

Integrating across memory episodes: Developmental trends

Memory enables us to use information from our past experiences to guide new behaviours, calling for the need to integrate or form inference across multiple distinct episodic experiences. Here, we compared children (aged 9-10 years), adolescents (aged 12-13 years), and young adults (aged 19-25 years) on their ability to form integration across overlapping associations in memory. Participants first encoded a set of overlapping, direct AB- and BC-associations (object-face and face-object pairs) as well as non-overlapping, unique DE-associations. They were then tested on these associations and inferential AC-associations. The experiment consisted of four such encoding/retrieval cycles, each consisting of different stimuli set. For accuracy on both unique and inferential associations, young adults were found to outperform teenagers, who in turn outperformed children. However, children were particularly slower than teenagers and young adults in making judgements during inferential than during unique associations. This suggests that children may rely more on making inferences during retrieval, by first retrieving the direct associations, followed by making the inferential judgement. Furthermore, young adults showed a higher correlation between accuracy in direct (AB, BC) and inferential AC-associations than children. This suggests that, young adults relied closely on AB- and BC-associations for making AC decisions, potentially by forming integrated ABC-triplets during encoding or retrieval. Taken together, our findings suggest that there may be an age-related shift in how information is integrated across experienced episodes, namely from relying on making inferences at retrieval during middle childhood to forming integrated representations at different memory processing stages in adulthood

Consolidation of vocabulary during sleep : the rich get richer?

Sleep plays a role in strengthening new words and integrating them with existing vocabulary knowledge, consistent with neural models of learning in which sleep supports hippocampal transfer to neocortical memory. Such models are based on adult research, yet neural maturation may mean that the mechanisms supporting word learning vary across development. Here, we propose a model in which children may capitalise on larger amounts of slow-wave sleep to support a greater demand on learning and neural reorganisation, whereas adults may benefit from a richer knowledge base to support consolidation. Such an argument is reinforced by the well-reported “Matthew effect”, whereby rich vocabulary knowledge is associated with better acquisition of new vocabulary. We present a meta-analysis that supports this association between children’s existing vocabulary knowledge and their integration of new words overnight. Whilst multiple mechanisms likely contribute to vocabulary consolidation and neural reorganisation across the lifespan, we propose that contributions of existing knowledge should be rigorously examined in developmental studies. Such research has potential to greatly enhance neural models of learning