Hippocampal Engrams Generate Variable Behavioral Responses and Brain-Wide Network States

Author:

Dorst Kaitlyn E.ORCID,Senne Ryan A.ORCID,Diep Anh H.,de Boer Antje R.ORCID,Suthard Rebecca L.ORCID,Leblanc Heloise,Ruesch Evan A.,Pyo Angela Y.,Skelton Sara,Carstensen Lucas C.ORCID,Malmberg Samantha,McKissick Olivia P.,Bladon John H.ORCID,Ramirez Steve

Abstract

Freezing is a defensive behavior commonly examined during hippocampal-mediated fear engram reactivation. How these cellular populations engage the brain and modulate freezing across varying environmental demands is unclear. To address this, we optogenetically reactivated a fear engram in the dentate gyrus subregion of the hippocampus across three distinct contexts in male mice. We found that there were differential amounts of light-induced freezing depending on the size of the context in which reactivation occurred: mice demonstrated robust light-induced freezing in the most spatially restricted of the three contexts but not in the largest. We then utilized graph theoretical analyses to identify brain-wide alterations in cFos expression during engram reactivation across the smallest and largest contexts. Our manipulations induced positive interregional cFos correlations that were not observed in control conditions. Additionally, regions spanning putative “fear” and “defense” systems were recruited as hub regions in engram reactivation networks. Lastly, we compared the network generated from engram reactivation in the small context with a natural fear memory retrieval network. Here, we found shared characteristics such as modular composition and hub regions. By identifying and manipulating the circuits supporting memory function, as well as their corresponding brain-wide activity patterns, it is thereby possible to resolve systems-level biological mechanisms mediating memory's capacity to modulate behavioral states.

Funder

HHS | NIH | NIH Office of the Director

Ludwig Family Foundation

DOD | USAF | AMC | Air Force Office of Scientific Research

Pew Charitable Trusts

Evelyn F. McKnight Brain Research Foundation

Chan Zuckerberg Initiative

Publisher

Society for Neuroscience

Subject

General Neuroscience

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