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Hippocampal cells multiplex positive and negative engrams

Monika Shpokayte, Olivia McKissick, Bingbing Yuan, Bahar Rahsepar, Fernando R. Fernandez, Evan Ruesch, Stephanie L. Grella, John A. White, X. Shawn Liu, Steve Ramirez
doi: https://doi.org/10.1101/2020.12.11.419887
Monika Shpokayte
1Graduate Program for Neuroscience, Boston University, Boston, MA, 02215
5Department of Psychological and Brain Sciences, The Center for Systems Neuroscience, Neurophotonics Center, and Photonics Center, Boston University, Boston, MA, 02215
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Olivia McKissick
2Neuroscience Graduate Program, Brown University, Providence, RI, 02912
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Bingbing Yuan
3Whitehead Institute for Biomedical Research, MIT, Cambridge, MA, 02142
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Bahar Rahsepar
4Department of Biomedical Engineering, Boston University, Boston, MA, 02215
5Department of Psychological and Brain Sciences, The Center for Systems Neuroscience, Neurophotonics Center, and Photonics Center, Boston University, Boston, MA, 02215
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Fernando R. Fernandez
4Department of Biomedical Engineering, Boston University, Boston, MA, 02215
5Department of Psychological and Brain Sciences, The Center for Systems Neuroscience, Neurophotonics Center, and Photonics Center, Boston University, Boston, MA, 02215
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Evan Ruesch
5Department of Psychological and Brain Sciences, The Center for Systems Neuroscience, Neurophotonics Center, and Photonics Center, Boston University, Boston, MA, 02215
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Stephanie L. Grella
4Department of Biomedical Engineering, Boston University, Boston, MA, 02215
5Department of Psychological and Brain Sciences, The Center for Systems Neuroscience, Neurophotonics Center, and Photonics Center, Boston University, Boston, MA, 02215
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John A. White
4Department of Biomedical Engineering, Boston University, Boston, MA, 02215
5Department of Psychological and Brain Sciences, The Center for Systems Neuroscience, Neurophotonics Center, and Photonics Center, Boston University, Boston, MA, 02215
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X. Shawn Liu
6Department of Physiology and Cellular Biophysics, Columbia University Medical Center, New York, NY 10032
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  • For correspondence: sl4738@cumc.columbia.edu
Steve Ramirez
4Department of Biomedical Engineering, Boston University, Boston, MA, 02215
5Department of Psychological and Brain Sciences, The Center for Systems Neuroscience, Neurophotonics Center, and Photonics Center, Boston University, Boston, MA, 02215
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  • For correspondence: sl4738@cumc.columbia.edu
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Abstract

The hippocampus is involved in processing a variety of mnemonic computations including the spatiotemporal components, as well as the corresponding emotional dimensions, of contextual memory.1–3 Recent studies have demonstrated vast structural and functional heterogeneity along the dorsal-ventral axis4 of the hippocampus, and while much is known about how the dorsal hippocampus processes spatial-temporal content, much less is known about whether or not the ventral hippocampus (vHPC) partitions positive and negative experiences into distinct sets of cells.4–9 Here, we combine transgenic and all-virus based activity-dependent tagging strategies to visualize multiple valence-specific engrams in the vHPC and demonstrate two partially segregated, albeit physiologically similar, populations that respond to positive and negative experiences. Next, using an RNA Sequencing approach, we find that vHPC positive and negative engram cells display distinct transcriptional programs in which neurodegenerative- and neuroprotective-related gene sets are enriched, respectively. Additionally, while optogenetic manipulation of tagged cell bodies in vHPC is not sufficient to drive behavior, tagged vHPC terminals projecting to the amygdala and nucleus accumbens, but not the prefrontal cortex, have the capacity to drive preference and avoidance when stimulated, as well as to “switch” or “reset” their capacity to drive either, thereby demonstrating their flexible contributions to behavior. We conclude that the vHPC contains genetically, cellularly, and behaviorally distinct populations of cells processing positive and negative memory engrams. Together, our findings provide a novel means by which to visualize multiple engrams within the same brain and point to their unique genetic signatures as putative avenues for future therapeutic interventions.

One sentence summary The hippocampus contains neurons corresponding to positive and negative engrams, which are segregated by their molecular, cellular, and projection-specific features.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted December 11, 2020.
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Hippocampal cells multiplex positive and negative engrams
Monika Shpokayte, Olivia McKissick, Bingbing Yuan, Bahar Rahsepar, Fernando R. Fernandez, Evan Ruesch, Stephanie L. Grella, John A. White, X. Shawn Liu, Steve Ramirez
bioRxiv 2020.12.11.419887; doi: https://doi.org/10.1101/2020.12.11.419887
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Hippocampal cells multiplex positive and negative engrams
Monika Shpokayte, Olivia McKissick, Bingbing Yuan, Bahar Rahsepar, Fernando R. Fernandez, Evan Ruesch, Stephanie L. Grella, John A. White, X. Shawn Liu, Steve Ramirez
bioRxiv 2020.12.11.419887; doi: https://doi.org/10.1101/2020.12.11.419887

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