Current Biology
Volume 30, Issue 10, 18 May 2020, Pages 1821-1833.e8
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Article
Stress Disrupts Human Hippocampal-Prefrontal Function during Prospective Spatial Navigation and Hinders Flexible Behavior

https://doi.org/10.1016/j.cub.2020.03.006Get rights and content
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Highlights

  • Human participants engaged in a VR prospective navigational planning task

  • Psychological stress was manipulated post-learning during novel route planning

  • Cortical memory replay signals dynamically tracked prospective route planning

  • Stress disrupted memory and control circuitry and route neural replay and behavior

Summary

The ability to anticipate and flexibly plan for the future is critical for achieving goal-directed outcomes. Extant data suggest that neural and cognitive stress mechanisms may disrupt memory retrieval and restrict prospective planning, with deleterious impacts on behavior. Here, we examined whether and how acute psychological stress influences goal-directed navigational planning and efficient, flexible behavior. Our methods combined fMRI, neuroendocrinology, and machine learning with a virtual navigation planning task. Human participants were trained to navigate familiar paths in virtual environments and then (concurrent with fMRI) performed a planning and navigation task that could be most efficiently solved by taking novel shortcut paths. Strikingly, relative to non-stressed control participants, participants who performed the planning task under experimentally induced acute psychological stress demonstrated (1) disrupted neural activity critical for mnemonic retrieval and mental simulation and (2) reduced traversal of shortcuts and greater reliance on familiar paths. These neural and behavioral changes under psychological stress were tied to evidence for disrupted neural replay of memory for future locations in the spatial environment, providing mechanistic insight into why and how stress can alter planning and foster inefficient behavior.

Keywords

Memory
Stress
fMRI
Navigation
Hippocampus
Cognitive Control

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