Aging and the encoding of changes in events: The role of neural activity pattern reinstatement

Edited by Joshua B. Tenenbaum, Massachusetts Institute of Technology, Cambridge, MA, and accepted by Editorial Board Member Dale Purves July 28, 2020 (received for review October 16, 2019)
November 23, 2020
117 (47) 29346-29353

Abstract

When encountering unexpected event changes, memories of relevant past experiences must be updated to form new representations. Current models of memory updating propose that people must first generate memory-based predictions to detect and register that features of the environment have changed, then encode the new event features and integrate them with relevant memories of past experiences to form configural memory representations. Each of these steps may be impaired in older adults. Using functional MRI, we investigated these mechanisms in healthy young and older adults. In the scanner, participants first watched a movie depicting everyday activities in a day of an actor’s life. They next watched a second nearly identical movie in which some scenes ended differently. Crucially, before watching the last part of each activity, the second movie stopped, and participants were asked to mentally replay how the activity previously ended. Three days later, participants were asked to recall the activities. Neural activity pattern reinstatement in medial temporal lobe (MTL) during the replay phase of the second movie was associated with detecting changes and with better memory for the original activity features. Reinstatements in posterior medial cortex (PMC) additionally predicted better memory for changed features. Compared to young adults, older adults showed a reduced ability to detect and remember changes and weaker associations between reinstatement and memory performance. These findings suggest that PMC and MTL contribute to change processing by reinstating previous event features, and that older adults are less able to use reinstatement to update memory for changed features.

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Acknowledgments

We thank Ryan Kahle, Madeleine Schroedel, and Priscilla Mei for assistance with data collection and coding. We also thank Aaron B. Tanenbaum for his help with spatial preprocessing and selection of the fMRI sequences. This project was funded by NIH Grant R21AG05231401 and supported in part by the Neuroimaging Informatics and Analysis Center (1P30NS098577). D.S. is currently supported by the European Union’s Horizon 2020 Research and Innovation Programme under Marie Skłodowska‐Curie Grant Agreement no. 798109. J.A.E. was partially supported by National Institutes of Health Grant number R37MH066078.

Supporting Information

Appendix (PDF)

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Information & Authors

Information

Published in

The cover image for PNAS Vol.117; No.47
Proceedings of the National Academy of Sciences
Vol. 117 | No. 47
November 24, 2020
PubMed: 33229530

Classifications

Submission history

Published online: November 23, 2020
Published in issue: November 24, 2020

Keywords

  1. representational similarity analysis
  2. cognitive aging
  3. event cognition
  4. episodic memory
  5. change comprehension

Acknowledgments

We thank Ryan Kahle, Madeleine Schroedel, and Priscilla Mei for assistance with data collection and coding. We also thank Aaron B. Tanenbaum for his help with spatial preprocessing and selection of the fMRI sequences. This project was funded by NIH Grant R21AG05231401 and supported in part by the Neuroimaging Informatics and Analysis Center (1P30NS098577). D.S. is currently supported by the European Union’s Horizon 2020 Research and Innovation Programme under Marie Skłodowska‐Curie Grant Agreement no. 798109. J.A.E. was partially supported by National Institutes of Health Grant number R37MH066078.

Notes

This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “Brain Produces Mind by Modeling,” held May 1–3, 2019, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, CA. NAS colloquia began in 1991 and have been published in PNAS since 1995. From February 2001 through May 2019, colloquia were supported by a generous gift from The Dame Jillian and Dr. Arthur M. Sackler Foundation for the Arts, Sciences, & Humanities, in memory of Dame Sackler’s husband, Arthur M. Sackler. The complete program and video recordings of most presentations are available on the NAS website at http://www.nasonline.org/brain-produces-mind-by.
This article is a PNAS Direct Submission. J.B.T. is a guest editor invited by the Editorial Board.

Authors

Affiliations

David Stawarczyk1 [email protected]
Department of Psychological & Brain Sciences, Washington University in St. Louis, St. Louis, MO 63105;
Department of Psychology, Psychology and Neuroscience of Cognition Research Unit, University of Liège, 4000 Liège, Belgium;
Department of Psychology, University of North Carolina at Greensboro, Greensboro, NC 27412;
Department of Psychological & Brain Sciences, Washington University in St. Louis, St. Louis, MO 63105;
Mallinckrodt Institute of Radiology, Washington University in St. Louis, St. Louis, MO 63110;
Department of Neurology, Washington University in St. Louis, St. Louis, MO 63105
Department of Psychological & Brain Sciences, Washington University in St. Louis, St. Louis, MO 63105;
Mallinckrodt Institute of Radiology, Washington University in St. Louis, St. Louis, MO 63110;

Notes

1
To whom correspondence may be addressed. Email: [email protected].
Author contributions: D.S., C.N.W., J.A.E., and J.M.Z. designed research; D.S. performed research; J.A.E. and A.Z.S. contributed new reagents/analytic tools; D.S., J.A.E., and J.M.Z. analyzed data; and D.S., C.N.W., and J.M.Z. wrote the paper with contributions from J.A.E. and A.Z.S.

Competing Interests

The authors declare no competing interest.

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    Aging and the encoding of changes in events: The role of neural activity pattern reinstatement
    Proceedings of the National Academy of Sciences
    • Vol. 117
    • No. 47
    • pp. 29243-29991

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