Chemogenetic inhibition of prefrontal cortex inputs to dorsal raphe reduces anxiety behaviors in male rat model of fetal alcohol spectrum disorder

Abstract Prenatal ethanol exposure (PE) causes Fetal Alcohol Spectrum Disorders (FASD), characterized by cognitive, behavioral, and emotional deficits, including anxiety and depression. PE-induced alteration in the function of dorsal raphe nucleus (DRN) serotonin (5-HT) neurons is thought to be majo...

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Main Authors: Saida Oubraim, Kathryn Hausknecht, Veronika Micov, Roh-Yu Shen, Samir Haj-Dahmane
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-025-99181-8
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author Saida Oubraim
Kathryn Hausknecht
Veronika Micov
Roh-Yu Shen
Samir Haj-Dahmane
author_facet Saida Oubraim
Kathryn Hausknecht
Veronika Micov
Roh-Yu Shen
Samir Haj-Dahmane
author_sort Saida Oubraim
collection DOAJ
description Abstract Prenatal ethanol exposure (PE) causes Fetal Alcohol Spectrum Disorders (FASD), characterized by cognitive, behavioral, and emotional deficits, including anxiety and depression. PE-induced alteration in the function of dorsal raphe nucleus (DRN) serotonin (5-HT) neurons is thought to be major contributing factor for increased anxiety. However, the precise neuronal circuits involved are unknown. Using electrophysiology, optogenetics, chemogenetics, and behavioral approaches, we find that PE preferentially potentiates medial prefrontal cortex (mPFC) glutamatergic inputs, but not lateral habenula (LHb), to DRN 5-HT neurons projecting to mPFC. Additionally, PE also increases the strength of LHb but not mPFC excitatory inputs to DRN 5-HT neurons projecting to central amygdala (Ce). This input and target selective effect of PE was mediated by a circuit-specific increase in nitric oxide (NO) signaling. Importantly, chemogenetic inhibition of mPFC-DRN neuronal circuit blunted anxiety-like behaviors in PE rats. As such, our results unraveled the DRN neuronal circuitries affected by PE, which gate FASD-induced anxiety-like behaviors.
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spelling doaj-art-6aa8d2c5e2f64276b2b99e8bf89f0b7a2025-08-20T03:13:55ZengNature PortfolioScientific Reports2045-23222025-04-0115111510.1038/s41598-025-99181-8Chemogenetic inhibition of prefrontal cortex inputs to dorsal raphe reduces anxiety behaviors in male rat model of fetal alcohol spectrum disorderSaida Oubraim0Kathryn Hausknecht1Veronika Micov2Roh-Yu Shen3Samir Haj-Dahmane4Department of Pharmacology and Toxicology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New YorkDepartment of Pharmacology and Toxicology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New YorkDepartment of Pharmacology and Toxicology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New YorkDepartment of Pharmacology and Toxicology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New YorkDepartment of Pharmacology and Toxicology, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, State University of New YorkAbstract Prenatal ethanol exposure (PE) causes Fetal Alcohol Spectrum Disorders (FASD), characterized by cognitive, behavioral, and emotional deficits, including anxiety and depression. PE-induced alteration in the function of dorsal raphe nucleus (DRN) serotonin (5-HT) neurons is thought to be major contributing factor for increased anxiety. However, the precise neuronal circuits involved are unknown. Using electrophysiology, optogenetics, chemogenetics, and behavioral approaches, we find that PE preferentially potentiates medial prefrontal cortex (mPFC) glutamatergic inputs, but not lateral habenula (LHb), to DRN 5-HT neurons projecting to mPFC. Additionally, PE also increases the strength of LHb but not mPFC excitatory inputs to DRN 5-HT neurons projecting to central amygdala (Ce). This input and target selective effect of PE was mediated by a circuit-specific increase in nitric oxide (NO) signaling. Importantly, chemogenetic inhibition of mPFC-DRN neuronal circuit blunted anxiety-like behaviors in PE rats. As such, our results unraveled the DRN neuronal circuitries affected by PE, which gate FASD-induced anxiety-like behaviors.https://doi.org/10.1038/s41598-025-99181-8
spellingShingle Saida Oubraim
Kathryn Hausknecht
Veronika Micov
Roh-Yu Shen
Samir Haj-Dahmane
Chemogenetic inhibition of prefrontal cortex inputs to dorsal raphe reduces anxiety behaviors in male rat model of fetal alcohol spectrum disorder
Scientific Reports
title Chemogenetic inhibition of prefrontal cortex inputs to dorsal raphe reduces anxiety behaviors in male rat model of fetal alcohol spectrum disorder
title_full Chemogenetic inhibition of prefrontal cortex inputs to dorsal raphe reduces anxiety behaviors in male rat model of fetal alcohol spectrum disorder
title_fullStr Chemogenetic inhibition of prefrontal cortex inputs to dorsal raphe reduces anxiety behaviors in male rat model of fetal alcohol spectrum disorder
title_full_unstemmed Chemogenetic inhibition of prefrontal cortex inputs to dorsal raphe reduces anxiety behaviors in male rat model of fetal alcohol spectrum disorder
title_short Chemogenetic inhibition of prefrontal cortex inputs to dorsal raphe reduces anxiety behaviors in male rat model of fetal alcohol spectrum disorder
title_sort chemogenetic inhibition of prefrontal cortex inputs to dorsal raphe reduces anxiety behaviors in male rat model of fetal alcohol spectrum disorder
url https://doi.org/10.1038/s41598-025-99181-8
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