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Serotonin Modulates an Inhibitory Input to the Central Amygdala from the Ventral Periaqueductal Gray

Olivia J. Hon, Jeffrey F. DiBerto, Christopher M. Mazzone, Jonathan Sugam, View ORCID ProfileDaniel W. Bloodgood, J. Andrew Hardaway, Mariya Husain, Alexis Kendra, Nora M. McCall, Alberto J. Lopez, Thomas L. Kash, Emily G. Lowery-Gionta
doi: https://doi.org/10.1101/2022.03.28.486055
Olivia J. Hon
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
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Jeffrey F. DiBerto
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
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Christopher M. Mazzone
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
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Jonathan Sugam
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
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Daniel W. Bloodgood
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
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  • ORCID record for Daniel W. Bloodgood
J. Andrew Hardaway
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
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Mariya Husain
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
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Alexis Kendra
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
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Nora M. McCall
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
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Alberto J. Lopez
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
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Thomas L. Kash
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
2Department of Pharmacology, School of Medicine, University of North Carolina at Chapel Hill
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Emily G. Lowery-Gionta
1Bowles Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill
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  • For correspondence: emily.g.lowery-gionta.civ@mail.mil
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ABSTRACT

Fear is an adaptive state that drives defensive behavioral responses to specific and imminent threats. The central nucleus of the amygdala (CeA) is a critical site of adaptations that are required for the acquisition and expression of fear, in part due to alterations in the activity of inputs to the CeA. Here, we characterize a novel GABAergic input to the CeA from the ventral periaqueductal gray area (vPAG) using fiber photometry and ex vivo whole-cell slice electrophysiology combined with optogenetics and pharmacology. GABA transmission from this ascending vPAG-CeA input was enhanced by bath application of serotonin via activation of serotonin type 2C (5HT2C) receptors. Results indicate that these receptors are presynaptic. Interestingly, we found that GABA release from the vPAG-CeA input is enhanced following fear learning via activation of 5HT2C receptors and that this pathway is dynamically engaged during fear learning. Additionally, we characterized serotonin release in the CeA during fear learning and recall for the first time using fiber photometry coupled to a serotonin biosensor. Together, these findings describe a mechanism by which serotonin modulates GABA release from ascending vPAG GABA inputs to the CeA and characterize a role for this pathway in fear learning.

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-NC 4.0 International license.
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Posted March 29, 2022.
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Serotonin Modulates an Inhibitory Input to the Central Amygdala from the Ventral Periaqueductal Gray
Olivia J. Hon, Jeffrey F. DiBerto, Christopher M. Mazzone, Jonathan Sugam, Daniel W. Bloodgood, J. Andrew Hardaway, Mariya Husain, Alexis Kendra, Nora M. McCall, Alberto J. Lopez, Thomas L. Kash, Emily G. Lowery-Gionta
bioRxiv 2022.03.28.486055; doi: https://doi.org/10.1101/2022.03.28.486055
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Serotonin Modulates an Inhibitory Input to the Central Amygdala from the Ventral Periaqueductal Gray
Olivia J. Hon, Jeffrey F. DiBerto, Christopher M. Mazzone, Jonathan Sugam, Daniel W. Bloodgood, J. Andrew Hardaway, Mariya Husain, Alexis Kendra, Nora M. McCall, Alberto J. Lopez, Thomas L. Kash, Emily G. Lowery-Gionta
bioRxiv 2022.03.28.486055; doi: https://doi.org/10.1101/2022.03.28.486055

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