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Prepronociceptin expressing neurons in the extended amygdala encode and promote rapid arousal responses to motivationally salient stimuli

Jose Rodriguez-Romaguera, Randall L Ung, Hiroshi Nomura, James M Otis, Marcus L Basiri, Vijay MK Namboodiri, Xueqi Zhu, J Elliott Robinson, Jenna A McHenry, Oksana Kosyk, Thomas C Jhou, Thomas L Kash, Michael R Bruchas, Garret D Stuber
doi: https://doi.org/10.1101/2020.01.21.914341
Jose Rodriguez-Romaguera
Department of Psychiatry, University of North Carolina, Chapel Hill, NC
Neuroscience Center, University of North Carolina, Chapel Hill, NC
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Randall L Ung
Neuroscience Center, University of North Carolina, Chapel Hill, NC
Neuroscience Curriculum, University of North Carolina, Chapel Hill, NC
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Hiroshi Nomura
Department of Psychiatry, University of North Carolina, Chapel Hill, NC
Neuroscience Center, University of North Carolina, Chapel Hill, NC
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James M Otis
Department of Psychiatry, University of North Carolina, Chapel Hill, NC
Neuroscience Center, University of North Carolina, Chapel Hill, NC
Department of Neuroscience, Medical University of South Carolina, Charleston, SC 29425, USA
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Marcus L Basiri
Neuroscience Center, University of North Carolina, Chapel Hill, NC
Neuroscience Curriculum, University of North Carolina, Chapel Hill, NC
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Vijay MK Namboodiri
Department of Psychiatry, University of North Carolina, Chapel Hill, NC
Neuroscience Center, University of North Carolina, Chapel Hill, NC
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Xueqi Zhu
Department of Psychiatry, University of North Carolina, Chapel Hill, NC
Neuroscience Center, University of North Carolina, Chapel Hill, NC
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J Elliott Robinson
Neuroscience Center, University of North Carolina, Chapel Hill, NC
Neuroscience Curriculum, University of North Carolina, Chapel Hill, NC
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Jenna A McHenry
Department of Psychiatry, University of North Carolina, Chapel Hill, NC
Neuroscience Center, University of North Carolina, Chapel Hill, NC
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Oksana Kosyk
Department of Psychiatry, University of North Carolina, Chapel Hill, NC
Neuroscience Center, University of North Carolina, Chapel Hill, NC
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Thomas C Jhou
Department of Neuroscience, Medical University of South Carolina, Charleston, NC
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Thomas L Kash
Neuroscience Curriculum, University of North Carolina, Chapel Hill, NC
Bowles Center for Alcohol Studies, Department of Pharmacology, University of North Carolina, Chapel Hill, NC
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Michael R Bruchas
Department of Anesthesiology, Washington University Pain Center, Department of Neuroscience, Division of Biology and Biomedical Sciences, Department of Biomedical Engineering, Washington University, St. Louis, MO
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Garret D Stuber
Department of Psychiatry, University of North Carolina, Chapel Hill, NC
Neuroscience Center, University of North Carolina, Chapel Hill, NC
Neuroscience Curriculum, University of North Carolina, Chapel Hill, NC
Department of Cell Biology and Physiology, University of North Carolina, Chapel Hill, NC
Center for the Neurobiology of Addiction, Pain, and Emotion, Department of Anesthesiology and Pain Medicine & Department of Pharmacology, University of Washington, Seattle, WA
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  • For correspondence: gstuber@uw.edu
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ABSTRACT

Motivational states are complex and consist of cognitive, emotional, and physiological components controlled by a network across multiple brain regions. An integral component of this neural circuitry is the bed nucleus of the stria terminalis (BNST). Here, we identified a subpopulation of neurons within BNST expressing the gene prepronociceptin (PnocBNST), that can modulate the rapid changes in physiological arousal that occur upon exposure to stimuli with motivational salience. Using in vivo two-photon calcium imaging we found that excitatory responses from individual PnocBNST neurons directly corresponded with rapid increases in pupillary size and occurred upon exposure to both aversive and rewarding odors. Furthermore, optogenetic activation of these neurons increased pupillary size, but did not alter approach/avoidance or locomotor behaviors. These findings suggest that excitatory responses in PnocBNST neurons encode rapid arousal responses irrespective of tested behaviors. Further histological, electrophysiological, and single-cell RNA sequencing data revealed that PnocBNST neurons are composed of genetically and anatomically identifiable subpopulations that can be further investigated. Taken together, our findings demonstrate a key role for a PnocBNST neuronal ensemble in encoding the rapid arousal responses that are triggered by motivational stimuli.

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-ND 4.0 International license.
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Posted January 23, 2020.
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Prepronociceptin expressing neurons in the extended amygdala encode and promote rapid arousal responses to motivationally salient stimuli
Jose Rodriguez-Romaguera, Randall L Ung, Hiroshi Nomura, James M Otis, Marcus L Basiri, Vijay MK Namboodiri, Xueqi Zhu, J Elliott Robinson, Jenna A McHenry, Oksana Kosyk, Thomas C Jhou, Thomas L Kash, Michael R Bruchas, Garret D Stuber
bioRxiv 2020.01.21.914341; doi: https://doi.org/10.1101/2020.01.21.914341
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Prepronociceptin expressing neurons in the extended amygdala encode and promote rapid arousal responses to motivationally salient stimuli
Jose Rodriguez-Romaguera, Randall L Ung, Hiroshi Nomura, James M Otis, Marcus L Basiri, Vijay MK Namboodiri, Xueqi Zhu, J Elliott Robinson, Jenna A McHenry, Oksana Kosyk, Thomas C Jhou, Thomas L Kash, Michael R Bruchas, Garret D Stuber
bioRxiv 2020.01.21.914341; doi: https://doi.org/10.1101/2020.01.21.914341

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