Data-driven clustering of functional signals reveals gradients in processing both within the anterior hippocampus and across its long axis.

A particularly elusive puzzle concerning the hippocampus is how the structural differences along its long, anteroposterior axis might beget meaningful functional differences, particularly in terms of the granularity of information processing. One measure posits to quantify this granularity by calculating the average statistical independence of the BOLD signal across neighboring voxels, or inter-voxel similarity (IVS), and has shown the anterior hippocampus to process coarser-grained information than the posterior hippocampus. This measure, however, has yielded opposing results in studies of developmental and healthy aging samples, which also varied in fMRI acquisition parameters and hippocampal parcellation methods. In order to reconcile these findings, we measured IVS across two separate resting-state fMRI acquisitions and compared the results across many of the most widely used parcellation methods in a large young-adult sample of male and female humans (Acquisition 1, N = 233; Acquisition 2, N = 176). Finding conflicting results across acquisitions and parcellations, we reasoned that a data-driven approach to hippocampal parcellation is necessary. To this end, we implemented a group masked independent components analysis (mICA) to identify functional subunits of the hippocampus, most notably separating the anterior hippocampus into separate anterior-medial, anterior-lateral, and posteroanterior-lateral components. Measuring IVS across these components revealed a decrease in IVS along the medial-lateral axis of the anterior hippocampus but an increase from anterior to posterior. We conclude that inter-voxel similarity is deeply affected by parcellation, and that grounding one's parcellation in a functionally informed approach might allow for a more complex and reliable characterization of the hippocampus.SIGNIFICANCE STATEMENT:Processing information along hierarchical scales of granularity is critical for many of the feats of cognition considered most human. Recently, the changes in structure, cortical connectivity, and apparent functional properties across parcels of the hippocampal long axis have been hypothesized to underlie this hierarchical gradient in information processing. We show here, however, that the choice of parcellation method itself drastically affects one particular measure of granularity across the hippocampus, and that a functionally informed approach to parcellation reveals gradients both within the anterior hippocampus and in non-linear form across the long axis. These results point to the issue of parcellation as a critical one in the study of the hippocampus and reorient interpretation of existing results.

Cross-Modal Facilitation of Episodic Memory by Sequential Action Execution.

Throughout our lives, the actions we produce are often highly familiar and repetitive (e.g., commuting to work). However, layered upon these routine actions are novel, episodic experiences. Substantial research has shown that prior knowledge can facilitate learning of conceptually related new information. But despite the central role our behavior plays in real-world experience, it remains unclear how engagement in a familiar sequence of actions influences memory for unrelated, nonmotor information coincident with those actions. To investigate this, we had healthy young adults encode novel items while simultaneously following a sequence of actions (key presses) that was either predictable and well-learned or random. Across three experiments (N = 80 each), we found that temporal order memory, but not item memory, was significantly enhanced for novel items encoded while participants executed predictable compared with random action sequences. These results suggest that engaging in familiar behaviors during novel learning scaffolds within-event temporal memory, an essential feature of episodic experiences.

Age-Related Increases in Posterior Hippocampal Granularity Are Associated with Remote Detailed Episodic Memory in Development.

Episodic memory is critical to human functioning. In adults, episodic memory involves a distributed neural circuit in which the hippocampus plays a central role. As episodic memory abilities continue to develop across childhood and into adolescence, studying episodic memory maturation can provide insight into the development and construction of these hippocampal networks, and ultimately clues to their function in adulthood. While past developmental studies have shown that the hippocampus helps to support memory in middle childhood and adolescence, the extent to which ongoing maturation within the hippocampus contributes to developmental change in episodic memory abilities remains unclear. In contrast, slower maturing regions, such as the PFC, have been suggested to be the neurobiological locus of memory improvements into adolescence. However, it is also possible that the methods used to detect hippocampal development during middle childhood and adolescence are not sensitive enough. Here, we examine how temporal covariance (or differentiation) in voxel representations within anterior and posterior hippocampus change with age to support the development of detailed recollection in male and female developing humans. We find age-related increases in the distinctiveness of temporal activation profiles in the posterior, but not anterior, hippocampus. Second, we show that this measure of granularity, when present during postencoding rest periods, correlates with the recall of detailed memories of preceding stimuli several weeks postencoding, suggesting that granularity may promote memory stabilization.SIGNIFICANCE STATEMENT Studying hippocampal maturation can provide insight into episodic memory development, as well as clues to episodic functioning in adulthood. Past work has shown evidence both for and against hippocampal contributions to age-related improvements in memory performance, but has relied heavily on univariate approaches (averaging activity across hippocampal voxels), which may not be sensitive to nuanced developmental change. Here we use a novel approach, examining time signatures in individual hippocampal voxels to reveal regionally specific (anterior vs posterior hippocampus) differences in the distinctiveness (granularity) of temporal activation profiles across development. Importantly, posterior hippocampus granularity during windows of putative memory stabilization was associated with long-term memory specificity. This suggests that the posterior hippocampus gradually builds the capacity to support detailed episodic recall.

Predictions transform memories: How expected versus unexpected events are integrated or separated in memory.

Our brains constantly generate predictions about the environment based on prior knowledge. Many of the events we experience are consistent with these predictions, while others might be inconsistent with prior knowledge and thus violate our predictions. To guide future behavior, the memory system must be able to strengthen, transform, or add to existing knowledge based on the accuracy of our predictions. We synthesize recent evidence suggesting that when an event is consistent with our predictions, it leads to neural integration between related memories, which is associated with enhanced associative memory, as well as memory biases. Prediction errors, in turn, can promote both neural integration and separation, and lead to multiple mnemonic outcomes. We review these findings and how they interact with factors such as memory reactivation, prediction error strength, and task goals, to offer insight into what determines memory for events that violate our predictions. In doing so, this review brings together recent neural and behavioral research to advance our understanding of how predictions shape memory, and why.

Pupil-linked arousal signals track the temporal organization of events in memory.

Everyday life unfolds continuously, yet we tend to remember past experiences as discrete event sequences or episodes. Although this phenomenon has been well documented, the neuromechanisms that support the transformation of continuous experience into distinct and memorable episodes remain unknown. Here, we show that changes in context, or event boundaries, elicit a burst of autonomic arousal, as indexed by pupil dilation. Event boundaries also lead to the segmentation of adjacent episodes in later memory, evidenced by changes in memory for the temporal duration, order, and perceptual details of recent event sequences. These subjective and objective changes in temporal memory are also related to distinct temporal features of pupil dilations to boundaries as well as to the temporal stability of more prolonged pupil-linked arousal states. Collectively, our findings suggest that pupil measures reflect both stability and change in ongoing mental context representations, which in turn shape the temporal structure of memory.