Biology subjects

Preston, A. R.

Publications and source records attributed to Preston, A. R..

9 recordsLinked to original sources

bioRxiv2026

Children and adults use distinct neurocognitive mechanisms to support successful memory-based inference

Reasoning depends on the ability to connect information across distinct experiences to derive knowledge that was never directly observed, and this capacity exhibits protracted developmental improvement that extends into emerging adulthood. Despite extensive behavioral work, it remains unclear whether developmental gains in inference reflect quantitative strengthening of a single mechanism or qualitative changes in the knowledge representations and computations that support inference decisions. Here, we tested the hypothesis that improvements in inference are linked to maturation of the hippocampus and posterior parietal cortex, resulting in age-related differences in how inference decisions are computed. We predicted that children (7-12 years) would rely on an iterative retrieval mechanism, requiring retrieval and combination of multiple distinct memories at the time of inference, whereas adults would be able to directly retrieve inferred relationships from structured representations that encode shared relations across experiences. Using functional MRI combined with computational modeling of response times, we show that hippocampal activity predicts successful inference via an iterative retrieval mechanism in both children and adults. Critically, only in adults does angular gyrus activity predict inference via a distinct, direct retrieval mechanism, consistent with access to inferred relationships represented as either integrated memories or in geometrically aligned neural spaces that organize events according to their shared relational structure. These findings identify a developmental shift in the neural mechanisms that support inference, demonstrating that maturation of posterior parietal cortex enables access to representations that capture derived linkages across experiences, fundamentally changing how inference decisions are computed across development.

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bioRxiv2026

Hippocampal representations of temporal structure increase in scale and symmetry across development

Learning which experiences reliably co-occur in time is fundamental to episodic memory and improves markedly across childhood and adolescence. Although children and adults both engage the hippocampus while learning predictable sequences, the nature of the neural representations supporting statistical learning across development remains unknown. Here, we directly quantified item-level neural representations before and after children, early adolescents, and adults learned predictable temporal relationships between items, providing a direct measure of learning-related representational change. We identified three developmental shifts in hippocampal representation. First, although posterior hippocampus integrated temporally adjacent sequence elements similarly across age groups, integration of non-adjacent sequence elements increased with age in anterior hippocampus, indicating developmental expansion in the temporal scale of neural integration. Second, hippocampal representations changed in their directional organization, with children showing hippocampal representations reflecting only forward associations between adjacent events, whereas adolescents and adults exhibited bidirectional integration of sequence relationships. Third, functional connectivity between anterior hippocampus and frontoparietal cortex tracked statistical transition probabilities during learning and predicted memory performance. Together, these findings show that improvements in statistical learning during development reflect reorganization of hippocampal representations and hippocampal-cortical interactions, revealing how the developing brain constructs increasingly flexible representations of predictive temporal structure. HighlightsO_LIHippocampal representations of temporal sequences reorganize across development C_LIO_LITemporal integration expands from adjacent to non-adjacent events with age C_LIO_LISequence representations shift from forward-only to bidirectional integration C_LIO_LIHippocampal-frontoparietal connectivity predicts statistical learning ability C_LI

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bioRxiv2025

Development of anterior hippocampal integration underlies the protracted emergence of cognitive map formation and generalization

Flexible memory depends on cognitive maps that integrate spatial relationships and guide behavior as environments change. The anterior hippocampus is well positioned to support integration across broad spatiotemporal scales, but its late maturation may constrain development of flexible, map-based navigation. Here, we tested whether hippocampal temporal autocorrelation, an index of neural activity stability over time, tracks the development of spatial integration. In a large resting-state fMRI sample (N = 382; ages 5-34 years), temporal autocorrelation increased with age in anterior, but not posterior, hippocampus. This anterior-specific pattern was replicated in an independent task-based fMRI sample of children, adolescents, and adults (N = 85; aged 6-12 years and adults), wherein we linked hippocampal autocorrelation to dissociable components of spatial behavior. The navigation task separated memory for object locations from the ability to update and generalize knowledge across rotations of the distal reference frame and to new object sets. Although all age groups learned object locations, only older participants showed evidence that prior spatial structure supported performance as the environment changed across runs. Critically, hippocampal autocorrelation related to behavior only when spatial knowledge was used across runs, rather than improved through within-run feedback, with the clearest profile emerging in adults. In adults, anterior and posterior autocorrelation jointly predicted precise object-location memory, whereas anterior autocorrelation uniquely predicted efficient trajectories from novel starting positions. These findings identify anterior hippocampal temporal autocorrelation as a later-maturing computation that supports the transition from local spatial learning in childhood to flexible navigation through changing environments in adulthood. Significance StatementFinding our way through the world requires more than remembering where things are. We also need to use what we have learned to take new routes, adjust when familiar places change, and apply old knowledge to new situations. These abilities improve from childhood to adulthood, but the brain changes that support this transition remain unclear. We show that a signal in anterior hippocampus, a brain region important for linking experiences, becomes more stable over development. Using a navigation task that separated remembering object locations from flexibly using a map, we found that this signal was most strongly tied to adults ability to navigate efficiently through changing environments. These findings reveal a hippocampal mechanism that supports flexible navigation as children mature.

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bioRxiv2025

Efficient uniform sampling explains non-uniform memory of narrative stories

Humans do not remember all experiences uniformly. We remember certain moments better than others, and central gist better than detail. Current theories focus exclusively on surprise to explain why some moments are better remembered, and do not explain gist memory. We propose that humans uniformly sample incoming information in time, which explains both non-uniform memory and gist. Rather than surprise, this model predicts that the mutual information between a given moment and the rest of the experience drives memory. To test this model, participants listened to narrative stories and recalled them immediately afterward. Using large language models to quantify the information structure of narrative stories and participants recall, we found that our parsimonious uniform sampling model explained memory better than earlier theories. These findings suggest an alternative, simpler account of human memory that does not rely on costly feedback mechanisms for prioritizing encoding of specific information.

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bioRxiv2024

Distinct hippocampal mechanisms support concept formation and updating

Learning systems must constantly decide whether to create new representations or update existing ones. For example, a child learning that a bat is a mammal and not a bird would be best served by creating a new representation, whereas updating may be best when encountering a second similar bat. Characterizing the neural dynamics that underlie these complementary memory operations requires identifying the exact moments when each operation occurs. We address this challenge by interrogating fMRI brain activation with a computational learning model that predicts trial-by-trial when memories are created versus updated. We found distinct neural engagement in anterior hippocampus and ventral striatum for model-predicted memory create and update events during early learning. Notably, the degree of this effect in hippocampus, but not ventral striatum, significantly related to learning outcome. Hippocampus additionally showed distinct patterns of functional coactivation with ventromedial prefrontal cortex and angular gyrus during memory creation and premotor cortex during memory updating. These findings suggest that complementary memory functions, as formalized in computational learning models, underlie the rapid formation of novel conceptual knowledge, with the hippocampus and its interactions with frontoparietal circuits playing a crucial role in successful learning. Significance statementHow do we reconcile new experiences with existing knowledge? Prominent theories suggest that novel information is either captured by creating new memories or leveraged to update existing memories, yet empirical support of how these distinct memory operations unfold during learning is limited. Here, we combine computational modeling of human learning behaviour with functional neuroimaging to identify moments of memory formation and updating and characterize their neural signatures. We find that both hippocampus and ventral striatum are distinctly engaged when memories are created versus updated; however, it is only hippocampus activation that is associated with learning outcomes. Our findings motivate a key theoretical refinement that positions hippocampus is a key player in building organized memories from the earliest moments of learning.

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bioRxiv2023

Differentiation of related events in hippocampus supports memory reinstatement in development

Adults are capable of either differentiating or integrating similar events in memory based on which representations are optimal for a given situation. Yet how children represent related memories remains unknown. Here, children (7-10 years) and adults formed memories for separate yet overlapping events. We then measured how successfully remembered events were represented and reinstated using functional magnetic resonance imaging (fMRI). We found that children formed differentiated representations in hippocampus--such that related events were stored as less similar to one another compared to unrelated events. Conversely, adults formed integrated representations, wherein related events were stored as more similar, including in medial prefrontal cortex (mPFC). Furthermore, hippocampal differentiation among children and mPFC integration among adults tracked neocortical reinstatement of the specific features associated with the individual events. Together, these findings reveal that the same memory behaviors are supported by different underlying representations across development. Specifically, whereas differentiation underlies memory organization and retrieval in childhood, integration exhibits a protracted developmental trajectory.

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bioRxiv2021

Representations of temporal community structure in hippocampus and precuneus predict inductive reasoning decisions

Our understanding of the world is shaped by inferences about underlying structure. For example, at the gym, you might notice that the same people tend to arrive around the same time and infer that they are friends that work out together. Consistent with this idea, after participants are presented with a temporal sequence of objects that follows an underlying community structure, they are biased to infer that objects from the same community share the same properties. Here, we used fMRI to measure neural representations of objects after temporal community structure learning and examine how these representations support inference about object relationships. We found that community structure learning affected inferred object similarity: when asked to spatially group items based on their experience, participants tended to group together objects from the same community. Neural representations in perirhinal cortex predicted individual differences in object grouping, suggesting that high-level object representations are affected by temporal community learning. Furthermore, participants were biased to infer that objects from the same community would share the same properties. Using computational modeling of temporal learning and inference decisions, we found that inductive reasoning is influenced by both detailed knowledge of temporal statistics and abstract knowledge of the temporal communities. The fidelity of temporal community representations in hippocampus and precuneus predicted the degree to which temporal community membership biased reasoning decisions. Our results suggest that temporal knowledge is represented at multiple levels of abstraction, and that perirhinal cortex, hippocampus, and precuneus may support inference based on this knowledge.

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bioRxiv2018

Predictability changes what we remember in familiar temporal contexts

The human brain constantly anticipates the future based on memories of the past. Encountering a familiar situation reactivates memory of previous encounters which can trigger a prediction of what comes next to facilitate responsiveness. However, a prediction error can lead to pruning of the offending memory, a process that weakens its representation in the brain and leads to forgetting. Our goal in this study was to evaluate whether memories are spared from pruning in situations that allow for more abstract yet reliable predictions. We hypothesized that when the category, but not the identity, of a new stimulus can be anticipated, this will reduce pruning of existing memories and also reduce encoding of the specifics of new memories. Participants viewed a sequence of objects, some of which reappeared multiple times ("cues"), followed always by novel items. Half of the cues were followed by new items from different (unpredictable) categories, while others were followed by new items from a single (predictable) category. Pattern classification of fMRI data was used to identify category-specific predictions after each cue. Pruning was observed only in unpredictable contexts, while encoding of new items suffered more in predictable contexts. These findings demonstrate that how episodic memories are updated is influenced by the reliability of abstract-level predictions in familiar contexts.

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bioRxiv2017

Medial prefrontal cortex compresses concept representations through learning

Prefrontal cortex (PFC) is thought to support the ability to focus on goal-relevant information by filtering out irrelevant information, a process akin to dimensionality reduction. Here, we test this dimensionality reduction hypothesis by combining a data-driven approach to characterizing the complexity of neural representation with a theoretically-supported computational model of learning. We find strong evidence of goal-directed dimensionality reduction within human ventromedial PFC during learning. Importantly, by using model predictions of each participants attentional strategies during learning, we find that that the degree of neural compression predicts an individuals ability to selectively attend to concept-specific information. These findings suggest a domain-general mechanism of learning through compression in ventromedial PFC.

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