A neural code for time and space in the human brain

Time and space are primary dimensions of human experience. Separate lines of investigation have identified neural correlates of time and space, yet little is known about how these representations converge during self-guided experience. Here, 10 subjects with intracranially implanted microelectrodes...

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Published inCell reports (Cambridge) Vol. 42; no. 11; p. 113238
Main Authors Schonhaut, Daniel R., Aghajan, Zahra M., Kahana, Michael J., Fried, Itzhak
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 28.11.2023
Elsevier
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Online AccessGet full text
ISSN2211-1247
2211-1247
DOI10.1016/j.celrep.2023.113238

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Abstract Time and space are primary dimensions of human experience. Separate lines of investigation have identified neural correlates of time and space, yet little is known about how these representations converge during self-guided experience. Here, 10 subjects with intracranially implanted microelectrodes play a timed, virtual navigation game featuring object search and retrieval tasks separated by fixed delays. Time cells and place cells activate in parallel during timed navigation intervals, whereas a separate time cell sequence spans inter-task delays. The prevalence, firing rates, and behavioral coding strengths of time cells and place cells are indistinguishable—yet time cells selectively remap between search and retrieval tasks, while place cell responses remain stable. Thus, the brain can represent time and space as overlapping but dissociable dimensions. Time cells and place cells may constitute a biological basis for the cognitive map of spatiotemporal context onto which memories are written. [Display omitted] •Human medial temporal lobe and prefrontal cortex neurons encode time during task-free delays•Time and place are independently represented during timed navigation•Time cells remap between contextually similar events with stable place cell firing•Population neural activity represents time across multiple events in a sequence Schonhaut et al. record direct neural firing while subjects play a timed, virtual navigation game with object search and retrieval tasks separated by fixed delays. The authors find that neural codes for time and space are simultaneously active, context-specific, and dissociable, providing a putative mechanism for representing spatiotemporal context.
AbstractList Time and space are primary dimensions of human experience. Separate lines of investigation have identified neural correlates of time and space, yet little is known about how these representations converge during self-guided experience. Here, 10 subjects with intracranially implanted microelectrodes play a timed, virtual navigation game featuring object search and retrieval tasks separated by fixed delays. Time cells and place cells activate in parallel during timed navigation intervals, whereas a separate time cell sequence spans inter-task delays. The prevalence, firing rates, and behavioral coding strengths of time cells and place cells are indistinguishable−yet time cells selectively remap between search and retrieval tasks, while place cell responses remain stable. Thus, the brain can represent time and space as overlapping but dissociable dimensions. Time cells and place cells may constitute a biological basis for the cognitive map of spatiotemporal context onto which memories are written. Schonhaut et al. record direct neural firing while subjects play a timed, virtual navigation game with object search and retrieval tasks separated by fixed delays. The authors find that neural codes for time and space are simultaneously active, context-specific, and dissociable, providing a putative mechanism for representing spatiotemporal context.
Time and space are primary dimensions of human experience. Separate lines of investigation have identified neural correlates of time and space, yet little is known about how these representations converge during self-guided experience. Here, 10 subjects with intracranially implanted microelectrodes play a timed, virtual navigation game featuring object search and retrieval tasks separated by fixed delays. Time cells and place cells activate in parallel during timed navigation intervals, whereas a separate time cell sequence spans inter-task delays. The prevalence, firing rates, and behavioral coding strengths of time cells and place cells are indistinguishable-yet time cells selectively remap between search and retrieval tasks, while place cell responses remain stable. Thus, the brain can represent time and space as overlapping but dissociable dimensions. Time cells and place cells may constitute a biological basis for the cognitive map of spatiotemporal context onto which memories are written.Time and space are primary dimensions of human experience. Separate lines of investigation have identified neural correlates of time and space, yet little is known about how these representations converge during self-guided experience. Here, 10 subjects with intracranially implanted microelectrodes play a timed, virtual navigation game featuring object search and retrieval tasks separated by fixed delays. Time cells and place cells activate in parallel during timed navigation intervals, whereas a separate time cell sequence spans inter-task delays. The prevalence, firing rates, and behavioral coding strengths of time cells and place cells are indistinguishable-yet time cells selectively remap between search and retrieval tasks, while place cell responses remain stable. Thus, the brain can represent time and space as overlapping but dissociable dimensions. Time cells and place cells may constitute a biological basis for the cognitive map of spatiotemporal context onto which memories are written.
Time and space are primary dimensions of human experience. Separate lines of investigation have identified neural correlates of time and space, yet little is known about how these representations converge during self-guided experience. Here, 10 subjects with intracranially implanted microelectrodes play a timed, virtual navigation game featuring object search and retrieval tasks separated by fixed delays. Time cells and place cells activate in parallel during timed navigation intervals, whereas a separate time cell sequence spans inter-task delays. The prevalence, firing rates, and behavioral coding strengths of time cells and place cells are indistinguishable—yet time cells selectively remap between search and retrieval tasks, while place cell responses remain stable. Thus, the brain can represent time and space as overlapping but dissociable dimensions. Time cells and place cells may constitute a biological basis for the cognitive map of spatiotemporal context onto which memories are written. [Display omitted] •Human medial temporal lobe and prefrontal cortex neurons encode time during task-free delays•Time and place are independently represented during timed navigation•Time cells remap between contextually similar events with stable place cell firing•Population neural activity represents time across multiple events in a sequence Schonhaut et al. record direct neural firing while subjects play a timed, virtual navigation game with object search and retrieval tasks separated by fixed delays. The authors find that neural codes for time and space are simultaneously active, context-specific, and dissociable, providing a putative mechanism for representing spatiotemporal context.
Time and space are primary dimensions of human experience. Separate lines of investigation have identified neural correlates of time and space, yet little is known about how these representations converge during self-guided experience. Here, 10 subjects with intracranially implanted microelectrodes play a timed, virtual navigation game featuring object search and retrieval tasks separated by fixed delays. Time cells and place cells activate in parallel during timed navigation intervals, whereas a separate time cell sequence spans inter-task delays. The prevalence, firing rates, and behavioral coding strengths of time cells and place cells are indistinguishable—yet time cells selectively remap between search and retrieval tasks, while place cell responses remain stable. Thus, the brain can represent time and space as overlapping but dissociable dimensions. Time cells and place cells may constitute a biological basis for the cognitive map of spatiotemporal context onto which memories are written.
ArticleNumber 113238
Author Fried, Itzhak
Schonhaut, Daniel R.
Aghajan, Zahra M.
Kahana, Michael J.
AuthorAffiliation 2 Department of Neurosurgery, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90095, USA
5 Faculty of Medicine, Tel-Aviv University, Tel-Aviv 69978, Israel
3 Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104, USA
4 Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, Los Angeles, CA 90024, USA
1 Department of Neuroscience, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
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Issue 11
Keywords medial temporal lobe
virtual navigation
memory
human neurons
hippocampus
CP: Neuroscience
prefrontal cortex
time
Language English
License This is an open access article under the CC BY-NC-ND license.
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AUTHOR CONTRIBUTIONS
D.R.S. and M.J.K. conceived the study and designed the experiment. D.R.S., M.J.K., and I.F. acquired funding for the experiment. I.F. performed the surgeries, supervised data collection, and localized the electrodes. D.R.S. programmed the experiment, processed the data, analyzed the data, and created the visualizations. Z.M.A., M.J.K., and I.F. supervised the analysis. D.R.S. wrote the original draft of the paper. D.R.S., Z.M.A., M.J.K., and I.F. edited and revised the paper.
These authors contributed equally
Lead contact
ORCID 0000-0001-8667-031X
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Snippet Time and space are primary dimensions of human experience. Separate lines of investigation have identified neural correlates of time and space, yet little is...
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SubjectTerms Brain - physiology
CP: Neuroscience
hippocampus
Hippocampus - physiology
human neurons
Humans
medial temporal lobe
memory
Neurons - physiology
prefrontal cortex
Space Perception - physiology
time
virtual navigation
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Title A neural code for time and space in the human brain
URI https://dx.doi.org/10.1016/j.celrep.2023.113238
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