The Primate Hippocampus Constructs a Temporal Scaffold Anchored to Behavioral Events

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Abstract The hippocampus has been attributed a range of divergent functions, including roles in memory and navigation, but how its moment-to-moment neuronal activity supports cognition remains poorly understood. The activity of individual hippocampal neurons is correlated with numerous perceptual features and task variables, raising the question of whether these response properties reflect distinct mechanisms or support a single generalized computation. Here, we show that these diverse response properties reflect a unified organizing principle in which the hippocampus segments experience into discrete events, with population activity transitioning between discrete neural states at behaviorally salient moments. Recording from monkeys performing a virtual spatial alternation task, we found that population activity did not evolve smoothly over time but instead shifted abruptly at each relevant event. These discontinuities segmented activity into distinct ensembles, effectively chunking separate task epochs. Notably, many neuronal responses persisted across visually distinct environments, demonstrating that these dynamics reflect abstract task structure rather than specific sensory features. These results reveal that the hippocampus constructs a temporal scaffold anchored to relevant behavioral events, with each neural state tracking a distinct task phase. This organizational principle may explain the diverse neural correlates observed across studies: rather than individually encoding perceptual or behavioral variables, hippocampal neurons collectively signal the current phase of a behavioral sequence. Our findings suggest that the hippocampus parses experience into meaningful elements and tracks "position" within a learned behavioral structure.
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The Primate Hippocampus Constructs a Temporal Scaffold Anchored to Behavioral Events | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Biological Sciences - Article The Primate Hippocampus Constructs a Temporal Scaffold Anchored to Behavioral Events Jon Rueckemann, Yoni Browning, Autumn Mallory, Brian Kim, Adrienne Fairhall, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-8689485/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted You are reading this latest preprint version Abstract The hippocampus has been attributed a range of divergent functions, including roles in memory and navigation, but how its moment-to-moment neuronal activity supports cognition remains poorly understood. The activity of individual hippocampal neurons is correlated with numerous perceptual features and task variables, raising the question of whether these response properties reflect distinct mechanisms or support a single generalized computation. Here, we show that these diverse response properties reflect a unified organizing principle in which the hippocampus segments experience into discrete events, with population activity transitioning between discrete neural states at behaviorally salient moments. Recording from monkeys performing a virtual spatial alternation task, we found that population activity did not evolve smoothly over time but instead shifted abruptly at each relevant event. These discontinuities segmented activity into distinct ensembles, effectively chunking separate task epochs. Notably, many neuronal responses persisted across visually distinct environments, demonstrating that these dynamics reflect abstract task structure rather than specific sensory features. These results reveal that the hippocampus constructs a temporal scaffold anchored to relevant behavioral events, with each neural state tracking a distinct task phase. This organizational principle may explain the diverse neural correlates observed across studies: rather than individually encoding perceptual or behavioral variables, hippocampal neurons collectively signal the current phase of a behavioral sequence. Our findings suggest that the hippocampus parses experience into meaningful elements and tracks "position" within a learned behavioral structure. Biological sciences/Neuroscience/Learning and memory/Hippocampus Biological sciences/Neuroscience/Neural circuits Full Text Additional Declarations There is NO Competing Interest. Supplementary Files SuppMovie2TaskProgressionMeann10trials.mp4 Supplemental Video 2 - Mean population trajectory and structured variability across task epochs of individual pseudotrials SuppMovie1Behavior.mp4 Supplementary Video 1 - First-person view of the immersive virtual alternation task. SuppMovie3TaskProgression500trials.mp4 Supplemental Video 3 - Task-epoch structured hippocampal population trajectories SuppMovie4AgnosticClustering.mp4 Supplemental Video 4 - Behavior-agnostic clustering of population state space trajectories Cite Share Download PDF Status: Under Review Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. 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