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Research Article

Modulation of hippocampal brain networks produces changes in episodic simulation and divergent thinking

View ORCID ProfilePreston P. Thakral, Kevin P. Madore, View ORCID ProfileSarah E. Kalinowski, and View ORCID ProfileDaniel L. Schacter
PNAS June 9, 2020 117 (23) 12729-12740; first published May 26, 2020; https://doi.org/10.1073/pnas.2003535117
Preston P. Thakral
aDepartment of Psychology, Harvard University, Cambridge, MA 02138;
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  • ORCID record for Preston P. Thakral
  • For correspondence: prestonthakral@fas.harvard.edu dls@wjh.harvard.edu
Kevin P. Madore
bDepartment of Psychology, Stanford University, Stanford, CA 94305
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Sarah E. Kalinowski
aDepartment of Psychology, Harvard University, Cambridge, MA 02138;
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Daniel L. Schacter
aDepartment of Psychology, Harvard University, Cambridge, MA 02138;
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  • ORCID record for Daniel L. Schacter
  • For correspondence: prestonthakral@fas.harvard.edu dls@wjh.harvard.edu
  1. Contributed by Daniel L. Schacter, April 3, 2020 (sent for review February 25, 2020; reviewed by Roberto Cabeza and Joel L. Voss)

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Significance

Studies have suggested a role for episodic memory in imagining future events and thinking creatively. Here, we tested the causal role played by episodic memory in future imagining and creative thinking by using fMRI-guided transcranial magnetic stimulation to disrupt neural activity in the hippocampus, a brain region involved in episodic memory. After transcranial magnetic stimulation, participants generated fewer episodic details when imagining future events and produced fewer creative ideas. fMRI analyses revealed that these behavioral reductions were linked to a reduction in hippocampal activity. Our findings have implications for brain targets and interventions to alleviate declines in memory, imagination, creativity, and other sorts of adaptive episodic functioning.

Abstract

Prior functional magnetic resonance imaging (fMRI) studies indicate that a core network of brain regions, including the hippocampus, is jointly recruited during episodic memory, episodic simulation, and divergent creative thinking. Because fMRI data are correlational, it is unknown whether activity increases in the hippocampus, and the core network more broadly, play a causal role in episodic simulation and divergent thinking. Here we employed fMRI-guided transcranial magnetic stimulation (TMS) to assess whether temporary disruption of hippocampal brain networks impairs both episodic simulation and divergent thinking. For each of two TMS sessions, continuous θ-burst stimulation (cTBS) was applied to either a control site (vertex) or to a left angular gyrus target region. The target region was identified on the basis of a participant-specific resting-state functional connectivity analysis with a hippocampal seed region previously associated with memory, simulation, and divergent thinking. Following cTBS, participants underwent fMRI and performed a simulation, divergent thinking, and nonepisodic control task. cTBS to the target region reduced the number of episodic details produced for the simulation task and reduced idea production on divergent thinking. Performance in the control task did not statistically differ as a function of cTBS site. fMRI analyses revealed a selective and simultaneous reduction in hippocampal activity during episodic simulation and divergent thinking following cTBS to the angular gyrus versus vertex but not during the nonepisodic control task. Our findings provide evidence that hippocampal-targeted TMS can specifically modulate episodic simulation and divergent thinking, and suggest that the hippocampus is critical for these cognitive functions.

  • episodic memory
  • creativity
  • imagination
  • TMS
  • fMRI

Footnotes

  • ↵1To whom correspondence may be addressed. Email: prestonthakral{at}fas.harvard.edu or dls{at}wjh.harvard.edu.
  • Author contributions: P.P.T., K.P.M., and D.L.S. designed research; P.P.T. and S.E.K. performed research; P.P.T., K.P.M., and S.E.K. analyzed data; and P.P.T., K.P.M., S.E.K., and D.L.S. wrote the paper.

  • Reviewers: R.C., Duke University; and J.L.V., Northwestern University Feinberg School of Medicine.

  • The authors declare no competing interest.

  • See online for related content such as Commentaries.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2003535117/-/DCSupplemental.

Published under the PNAS license.

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Modulation of hippocampal brain networks produces changes in episodic simulation and divergent thinking
Preston P. Thakral, Kevin P. Madore, Sarah E. Kalinowski, Daniel L. Schacter
Proceedings of the National Academy of Sciences Jun 2020, 117 (23) 12729-12740; DOI: 10.1073/pnas.2003535117

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Modulation of hippocampal brain networks produces changes in episodic simulation and divergent thinking
Preston P. Thakral, Kevin P. Madore, Sarah E. Kalinowski, Daniel L. Schacter
Proceedings of the National Academy of Sciences Jun 2020, 117 (23) 12729-12740; DOI: 10.1073/pnas.2003535117
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