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The human brain reactivates context-specific past information at event boundaries of naturalistic experiences

Nature Neuroscience volume 26, pages 1080–1089 (2023)Cite this article

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Abstract

Although we perceive the world in a continuous manner, our experience is partitioned into discrete events. However, to make sense of these events, they must be stitched together into an overarching narrative—a model of unfolding events. It has been proposed that such a stitching process happens in offline neural reactivations when rodents build models of spatial environments. Here we show that, while understanding a natural narrative, humans reactivate neural representations of past events. Similar to offline replay, these reactivations occur in the hippocampus and default mode network, where reactivations are selective to relevant past events. However, these reactivations occur, not during prolonged offline periods, but at the boundaries between ongoing narrative events. These results, replicated across two datasets, suggest reactivations as a candidate mechanism for binding temporally distant information into a coherent understanding of ongoing experience.

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Fig. 1: Analysis pipeline.
Fig. 2: Within-participant reactivation of remote past events at event boundaries.
Fig. 3: Between-participant reactivation of remote past events at event boundaries.
Fig. 4: Reactivation is specific to event boundaries—replication across datasets.
Fig. 5: Relevant past events are preferentially reactivated at event boundaries.

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Data availability

Data underlying the findings of this study are available at https://dataspace.princeton.edu/handle/88435/dsp01nz8062179 and https://openneuro.org/datasets/ds002345/versions/1.1.4.

Code availability

Matlab code is available at https://osf.io/crmdb/.

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Acknowledgements

We would like to thank M. Behrmann, A. Ben-Yakov and T. Makin for their valuable insights, which greatly contributed to the manuscript. This work was supported by the European Molecular Biology Organization nonstipendiary Long-Term Fellowship (848–2017), Human Frontier Science Program (LT000444/2018), Israeli National Postdoctoral Award Program for Advancing Women in Science, and the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie Grant Agreement No. 789040 (to A.H.), the Blavatnik Postdoctoral Fellowship and the research program Change is Key! of the Riksbankens Jubileumsfond (M21-0021) (to H.D.), and a Wellcome collaborator award (214314/Z/18/Z), a Wellcome Trust Senior Research Fellowship (104765/Z/14/Z) and a Principal Research Fellowship (219525/Z/19/Z), together with a James S. McDonnell Foundation Award (JSMF220020372) (to T.E.J.B.). This research was funded in whole, or in part, by the Wellcome Trust (Grant number 214314/Z/18/Z and 219525/Z/19/Z). For the purpose of open access, the author has applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission.

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Authors and Affiliations

  1. Wellcome Trust Centre for Neuroimaging, UCL Queen Square Institute of Neurology, University College London, London, UK

    Avital Hahamy & Timothy E. J. Behrens

  2. School of Electronic Engineering and Computer Science, Queen Mary University of London, London, UK

    Haim Dubossarsky

  3. Language Technology Laboratory, University of Cambridge, Cambridge, UK

    Haim Dubossarsky

  4. Wellcome Centre for Integrative Neuroimaging, University of Oxford, John Radcliffe Hospital, Oxford, UK

    Timothy E. J. Behrens

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A.H. conducted all analyses. H.D. assisted with natural language processing analyses. A.H., H.D. and T.E.J.B. interpreted the results. A.H. and T.E.J.B. wrote the manuscript. T.E.J.B. supervised the project.

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Correspondence to Avital Hahamy.

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Hahamy, A., Dubossarsky, H. & Behrens, T.E.J. The human brain reactivates context-specific past information at event boundaries of naturalistic experiences. Nat Neurosci 26, 1080–1089 (2023). https://doi.org/10.1038/s41593-023-01331-6

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