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Symposium Session 7 - Neural Time Machine: Temporal Organization of Experience in the Brain
Chair: Jie Zheng1; 1University of California, Davis
Presenters: James Antony, Regina Lapate, Jingyi Wang, Benjamin Kanter, Jie Zheng
Episodic memory depends on the brain’s ability to organize continuous experience into temporally structured representations. Yet, the neural mechanisms that support this organization—ranging from moment-to-moment sequence encoding to long-term spacing effects—remain incompletely understood. This symposium assembles work across species, methodologies, and levels of analysis to examine how the brain encodes, segments, and retrieves experiences in time. James Antony will present a neurobiologically grounded computational model of hippocampal–entorhinal circuits, showing how gradual representational drift across multiple timescales provides a mechanistic account of the spacing effect (the long-term memory benefit of distributing learning over time). Regina Lapate will discuss findings indicating that resting-state entorhinal cortex and hippocampal connectivity patterns systematically drift over time, revealing a spontaneous neural signature of elapsed time in humans. Benjamin Kanter will present large-scale recordings from the hippocampus and entorhinal cortex in freely-behaving rodents, identifying a hierarchical coding scheme for organizing events across multiple timescales. Jie Zheng will share single-neuron recordings from humans performing an order memory task, uncovering “order-selective cells” in medial temporal and prefrontal regions that flexibly encode both absolute and relative event order via theta phase coding, thereby weaving individual episodes into coherent temporal narratives. Together, these complementary perspectives—from computational modeling, human and rodent electrophysiology, and fMRI—converge on a unifying question: how does the brain transform continuous experience into structured memories situated in time? By integrating approaches across disciplines and species, this symposium provides new mechanistic insights into how temporal organization supports memory, learning, and the construction of meaningful life narratives.
Presentations
Memory out of context: Spacing effects and decontextualization in a computational model of the medial temporal lobe
James Antony1; 1California Polytechnic State University (Cal Poly), San Luis Obispo
Neural representations gradually change across multiple timescales. In this talk, we will argue that modeling this “drift” could help explain the spacing effect (the long-term benefit of distributed learning), whereby differences between stored and current temporal context activity patterns produce greater error-driven learning. We trained a neurobiologically realistic model of the entorhinal cortex and hippocampus to learn paired associates alongside temporal context vectors that drifted between learning episodes and/or before final retention intervals. In line with spacing effects, greater drift produced better model recall after longer retention intervals. Dissecting model mechanisms revealed that greater drift increased error-driven learning, strengthened weights in slower drifting temporal context neurons (temporal abstraction), and improved direct cue-target associations (decontextualization). Intriguingly, these results suggest that decontextualization—generally ascribed only to the neocortex—can occur within the hippocampus itself. Altogether, our findings provide a mechanistic formalization for established learning concepts like spacing effects and errors during learning.
The intrinsic time tracker: Temporal context is embedded in entorhinal and hippocampal functional connectivity patterns
Regina Lapate1, Jingyi Wang1; 1Department of Psychological & Brain Sciences, University of California, Santa Barbara
Task-evoked activity patterns in the entorhinal cortex (EC) and hippocampus track or reflect changes in temporal context at short and long timescales. But do intrinsic EC and hippocampal signals—in the absence of task demands—also reflect the passage of time? By leveraging a dense-sampling study in which two individuals underwent daily resting-state fMRI for 30 days, we found that the similarity of EC- and anterior-hippocampal-whole-brain resting connectivity patterns negatively correlated with the time interval between sessions—suggesting a spontaneous, slow-drifting neural signature of time in humans. Temporal drift followed an anterior-to-posterior gradient in the hippocampus and was stronger in anterolateral than posteromedial EC. Analysis of an independent densely-sampled group replicated these effects over a 60-day period, with evidence for temporal tracking at multiple timescales along the hippocampus. These findings reveal a resting-state connectivity signature that reflects the passage of time and follows a functional gradient along the hippocampal longitudinal axis.
Event structure sculpts neural population dynamics in the lateral entorhinal cortex
Benjamin Kanter1; 1Kavli Institute for Systems Neuroscience and Centre for Algorithms in the Cortex, Norwegian University of Science and Technology, Trondheim, Norway
Our experience of the world is a continuous stream of events that must be segmented and organized at multiple timescales. The neural mechanisms underlying this process remain unknown. In this work, we simultaneously recorded hundreds to thousands of neurons in the lateral entorhinal cortex of freely behaving rats. Neural population activity drifted continuously along a one-dimensional manifold during all behaviors and behavioral states, including sleep, which points to an intrinsic origin of the drift. In awake animals, boundaries between events were associated with discrete shifts in population dynamics, which segmented the neural activity into temporal units. During tasks with recurring temporal structure, activity traveled additionally in directions orthogonal to the drift, encoding event information across multiple timescales. The results identify a hierarchical coding scheme for organizing events in time.
Weaving Time Into Memory: Order-Selective Cells Tile Temporal Space and Predict Order Memory
Jie Zheng1,2; 1Department of Neurological Surgery, University of California, Davis, Davis, CA, USA, 2Department of Biomedical Engineering, University of California, Davis, Davis, CA, USA
Episodic memory depends not only on remembering individual events but also on recalling their temporal order. How neural circuits support this temporal organization remains unclear. We recorded neural activity in 20 patients with depth electrodes as they encoded and recalled memories of video clips of everyday events segmented by visual event boundaries. Among 965 neurons, we discovered order-selective cells (OSCs) in the hippocampus, amygdala, and orbitofrontal cortex that signaled specific event positions independent of content or duration. During encoding, OSCs show theta phase precession at event boundaries, with their spikes shifting systematically with ongoing brain rhythms, and stronger precession predicting better memory. During retrieval, OSC spike phases shifted according to the relative position of events within recalled sequences, revealing a flexible coding scheme for subsets of experiences. These results identify a neuronal substrate for encoding absolute and relative temporal order, providing mechanistic insight into how the brain weaves discrete episodes into coherent narratives.
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