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Dysregulation of Prefrontal Cortex-Mediated Slow-Evolving Limbic Dynamics Drives Stress-Induced Emotional Pathology

Circuits distributed across cortico-limbic brain regions compose the networks that mediate emotional behavior. The prefrontal cortex (PFC) regulates ultraslow (

Journal Title: Neuron (Cambridge Mass.), 2016, Vol.91 (2), p.439-452
Main Author: Hultman, Rainbo
Other Authors: Mague, Stephen D , Li, Qiang , Katz, Brittany M , Michel, Nadine , Lin, Lizhen , Wang, Joyce , David, Lisa K , Blount, Cameron , Chandy, Rithi , Carlson, David , Ulrich, Kyle , Carin, Lawrence , Dunson, David , Kumar, Sunil , Deisseroth, Karl , Moore, Scott D , Dzirasa, Kafui
Format: Electronic Article Electronic Article
Language: English
Subjects:
Quelle: Alma/SFX Local Collection
Publisher: United States: Elsevier Inc
ID: ISSN: 0896-6273
Link: https://www.ncbi.nlm.nih.gov/pubmed/27346529
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recordid: cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4986697
title: Dysregulation of Prefrontal Cortex-Mediated Slow-Evolving Limbic Dynamics Drives Stress-Induced Emotional Pathology
format: Article
creator:
  • Hultman, Rainbo
  • Mague, Stephen D
  • Li, Qiang
  • Katz, Brittany M
  • Michel, Nadine
  • Lin, Lizhen
  • Wang, Joyce
  • David, Lisa K
  • Blount, Cameron
  • Chandy, Rithi
  • Carlson, David
  • Ulrich, Kyle
  • Carin, Lawrence
  • Dunson, David
  • Kumar, Sunil
  • Deisseroth, Karl
  • Moore, Scott D
  • Dzirasa, Kafui
subjects:
  • Amygdala - physiopathology
  • Analysis
  • Animal behavior
  • Animals
  • Article
  • Behavior
  • Behavior, Animal - physiology
  • Biomedical engineering
  • Chronic Stress
  • Depression, Mental
  • Depressive Disorder, Major - physiopathology
  • Electrodes
  • Emotions - physiology
  • Job stress
  • Machine learning
  • major depressive disorder
  • Mental depression
  • Mice, Inbred C57BL
  • nervous system
  • Neural networks
  • Neurophysiology
  • Oscillations
  • Pathology
  • Prefrontal Cortex - pathology
  • Prefrontal Cortex - physiopathology
  • Software
  • Stress
  • Stress, Psychological - pathology
  • Synchrony
ispartof: Neuron (Cambridge, Mass.), 2016, Vol.91 (2), p.439-452
description: Circuits distributed across cortico-limbic brain regions compose the networks that mediate emotional behavior. The prefrontal cortex (PFC) regulates ultraslow (
language: eng
source: Alma/SFX Local Collection
identifier: ISSN: 0896-6273
fulltext: fulltext
issn:
  • 0896-6273
  • 1097-4199
url: Link


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titleDysregulation of Prefrontal Cortex-Mediated Slow-Evolving Limbic Dynamics Drives Stress-Induced Emotional Pathology
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creatorHultman, Rainbo ; Mague, Stephen D ; Li, Qiang ; Katz, Brittany M ; Michel, Nadine ; Lin, Lizhen ; Wang, Joyce ; David, Lisa K ; Blount, Cameron ; Chandy, Rithi ; Carlson, David ; Ulrich, Kyle ; Carin, Lawrence ; Dunson, David ; Kumar, Sunil ; Deisseroth, Karl ; Moore, Scott D ; Dzirasa, Kafui
creatorcontribHultman, Rainbo ; Mague, Stephen D ; Li, Qiang ; Katz, Brittany M ; Michel, Nadine ; Lin, Lizhen ; Wang, Joyce ; David, Lisa K ; Blount, Cameron ; Chandy, Rithi ; Carlson, David ; Ulrich, Kyle ; Carin, Lawrence ; Dunson, David ; Kumar, Sunil ; Deisseroth, Karl ; Moore, Scott D ; Dzirasa, Kafui
descriptionCircuits distributed across cortico-limbic brain regions compose the networks that mediate emotional behavior. The prefrontal cortex (PFC) regulates ultraslow (<1 Hz) dynamics across these networks, and PFC dysfunction is implicated in stress-related illnesses including major depressive disorder (MDD). To uncover the mechanism whereby stress-induced changes in PFC circuitry alter emotional networks to yield pathology, we used a multi-disciplinary approach including in vivo recordings in mice and chronic social defeat stress. Our network model, inferred using machine learning, linked stress-induced behavioral pathology to the capacity of PFC to synchronize amygdala and VTA activity. Direct stimulation of PFC-amygdala circuitry with DREADDs normalized PFC-dependent limbic synchrony in stress-susceptible animals and restored normal behavior. In addition to providing insights into MDD mechanisms, our findings demonstrate an interdisciplinary approach that can be used to identify the large-scale network changes that underlie complex emotional pathologies and the specific network nodes that can be used to develop targeted interventions. •Prefrontal cortex (PFC) oscillations synchronize with ultraslow limbic dynamics•PFC unit firing signals the synchronization state of amygdala (AMY) and ventral tegmental area (VTA)•Chronic stress selectively disrupts PFC-dependent regulation of AMY-VTA synchrony•PFC to AMY circuit stimulation recovers normal network function and behavior The complex mechanisms whereby multiple brain regions coordinate emotion remain tenebrous. Hultman et al. show that the prefrontal cortex (PFC) directly regulates beta oscillatory connectivity between multiple limbic brain regions. Stress-induced disruption of this PFC-dependent function yields pathological emotional behavior.
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subjectAmygdala - physiopathology ; Analysis ; Animal behavior ; Animals ; Article ; Behavior ; Behavior, Animal - physiology ; Biomedical engineering ; Chronic Stress ; Depression, Mental ; Depressive Disorder, Major - physiopathology ; Electrodes ; Emotions - physiology ; Job stress ; Machine learning ; major depressive disorder ; Mental depression ; Mice, Inbred C57BL ; nervous system ; Neural networks ; Neurophysiology ; Oscillations ; Pathology ; Prefrontal Cortex - pathology ; Prefrontal Cortex - physiopathology ; Software ; Stress ; Stress, Psychological - pathology ; Synchrony
ispartofNeuron (Cambridge, Mass.), 2016, Vol.91 (2), p.439-452
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descriptionCircuits distributed across cortico-limbic brain regions compose the networks that mediate emotional behavior. The prefrontal cortex (PFC) regulates ultraslow (<1 Hz) dynamics across these networks, and PFC dysfunction is implicated in stress-related illnesses including major depressive disorder (MDD). To uncover the mechanism whereby stress-induced changes in PFC circuitry alter emotional networks to yield pathology, we used a multi-disciplinary approach including in vivo recordings in mice and chronic social defeat stress. Our network model, inferred using machine learning, linked stress-induced behavioral pathology to the capacity of PFC to synchronize amygdala and VTA activity. Direct stimulation of PFC-amygdala circuitry with DREADDs normalized PFC-dependent limbic synchrony in stress-susceptible animals and restored normal behavior. In addition to providing insights into MDD mechanisms, our findings demonstrate an interdisciplinary approach that can be used to identify the large-scale network changes that underlie complex emotional pathologies and the specific network nodes that can be used to develop targeted interventions. •Prefrontal cortex (PFC) oscillations synchronize with ultraslow limbic dynamics•PFC unit firing signals the synchronization state of amygdala (AMY) and ventral tegmental area (VTA)•Chronic stress selectively disrupts PFC-dependent regulation of AMY-VTA synchrony•PFC to AMY circuit stimulation recovers normal network function and behavior The complex mechanisms whereby multiple brain regions coordinate emotion remain tenebrous. Hultman et al. show that the prefrontal cortex (PFC) directly regulates beta oscillatory connectivity between multiple limbic brain regions. Stress-induced disruption of this PFC-dependent function yields pathological emotional behavior.
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abstractCircuits distributed across cortico-limbic brain regions compose the networks that mediate emotional behavior. The prefrontal cortex (PFC) regulates ultraslow (<1 Hz) dynamics across these networks, and PFC dysfunction is implicated in stress-related illnesses including major depressive disorder (MDD). To uncover the mechanism whereby stress-induced changes in PFC circuitry alter emotional networks to yield pathology, we used a multi-disciplinary approach including in vivo recordings in mice and chronic social defeat stress. Our network model, inferred using machine learning, linked stress-induced behavioral pathology to the capacity of PFC to synchronize amygdala and VTA activity. Direct stimulation of PFC-amygdala circuitry with DREADDs normalized PFC-dependent limbic synchrony in stress-susceptible animals and restored normal behavior. In addition to providing insights into MDD mechanisms, our findings demonstrate an interdisciplinary approach that can be used to identify the large-scale network changes that underlie complex emotional pathologies and the specific network nodes that can be used to develop targeted interventions. •Prefrontal cortex (PFC) oscillations synchronize with ultraslow limbic dynamics•PFC unit firing signals the synchronization state of amygdala (AMY) and ventral tegmental area (VTA)•Chronic stress selectively disrupts PFC-dependent regulation of AMY-VTA synchrony•PFC to AMY circuit stimulation recovers normal network function and behavior The complex mechanisms whereby multiple brain regions coordinate emotion remain tenebrous. Hultman et al. show that the prefrontal cortex (PFC) directly regulates beta oscillatory connectivity between multiple limbic brain regions. Stress-induced disruption of this PFC-dependent function yields pathological emotional behavior.
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pmid27346529
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