Local Neuronal Synchronization in Frequent Nightmare Recallers and Healthy Controls: A Resting-State Functional Magnetic Resonance Imaging Study

Nightmares are highly dysphoric dreams that are well-remembered upon awakening. Frequent nightmares have been associated with psychopathology and emotional dysregulation, yet their neural mechanisms remain largely unknown. Our neurocognitive model posits that nightmares reflect dysfunction in a limb...

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Main Authors: Louis-Philippe Marquis, Sarah-Hélène Julien, Véronique Daneault, Cloé Blanchette-Carrière, Tyna Paquette, Michelle Carr, Jean-Paul Soucy, Jacques Montplaisir, Tore Nielsen
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2021.645255/full
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author Louis-Philippe Marquis
Louis-Philippe Marquis
Sarah-Hélène Julien
Sarah-Hélène Julien
Véronique Daneault
Véronique Daneault
Cloé Blanchette-Carrière
Cloé Blanchette-Carrière
Tyna Paquette
Michelle Carr
Jean-Paul Soucy
Jacques Montplaisir
Jacques Montplaisir
Tore Nielsen
Tore Nielsen
spellingShingle Louis-Philippe Marquis
Louis-Philippe Marquis
Sarah-Hélène Julien
Sarah-Hélène Julien
Véronique Daneault
Véronique Daneault
Cloé Blanchette-Carrière
Cloé Blanchette-Carrière
Tyna Paquette
Michelle Carr
Jean-Paul Soucy
Jacques Montplaisir
Jacques Montplaisir
Tore Nielsen
Tore Nielsen
Local Neuronal Synchronization in Frequent Nightmare Recallers and Healthy Controls: A Resting-State Functional Magnetic Resonance Imaging Study
Frontiers in Neuroscience
nightmares
parasomnias
brain imaging
distress
psychopathology
regional homogeneity
author_facet Louis-Philippe Marquis
Louis-Philippe Marquis
Sarah-Hélène Julien
Sarah-Hélène Julien
Véronique Daneault
Véronique Daneault
Cloé Blanchette-Carrière
Cloé Blanchette-Carrière
Tyna Paquette
Michelle Carr
Jean-Paul Soucy
Jacques Montplaisir
Jacques Montplaisir
Tore Nielsen
Tore Nielsen
author_sort Louis-Philippe Marquis
title Local Neuronal Synchronization in Frequent Nightmare Recallers and Healthy Controls: A Resting-State Functional Magnetic Resonance Imaging Study
title_short Local Neuronal Synchronization in Frequent Nightmare Recallers and Healthy Controls: A Resting-State Functional Magnetic Resonance Imaging Study
title_full Local Neuronal Synchronization in Frequent Nightmare Recallers and Healthy Controls: A Resting-State Functional Magnetic Resonance Imaging Study
title_fullStr Local Neuronal Synchronization in Frequent Nightmare Recallers and Healthy Controls: A Resting-State Functional Magnetic Resonance Imaging Study
title_full_unstemmed Local Neuronal Synchronization in Frequent Nightmare Recallers and Healthy Controls: A Resting-State Functional Magnetic Resonance Imaging Study
title_sort local neuronal synchronization in frequent nightmare recallers and healthy controls: a resting-state functional magnetic resonance imaging study
publisher Frontiers Media S.A.
series Frontiers in Neuroscience
issn 1662-453X
publishDate 2021-03-01
description Nightmares are highly dysphoric dreams that are well-remembered upon awakening. Frequent nightmares have been associated with psychopathology and emotional dysregulation, yet their neural mechanisms remain largely unknown. Our neurocognitive model posits that nightmares reflect dysfunction in a limbic-prefrontal circuit comprising medial prefrontal and anterior cingulate cortices, hippocampus, and amygdala. However, there is a paucity of studies that used brain imaging to directly test the neural correlates of nightmares. One such study compared the regional homogeneity (ReHo) of resting-state functional magnetic resonance imaging blood-oxygen level-dependent signals between frequent nightmare recallers and controls. The main results were greater regional homogeneity in the left anterior cingulate cortex and right inferior parietal lobule for the nightmare recallers than for the controls. In the present study, we aimed to document the ReHo correlates of frequent nightmares using several nightmare severity measures. We acquired resting-state functional magnetic resonance imaging data from 18 frequent nightmare recallers aged 18–35 (3 males and 15 females) and 18 age- and sex-matched controls, as well as retrospective and prospective disturbed dreaming frequency estimates and scores on the Nightmare Distress Questionnaire. While there were inconsistent results for our different analyses (group comparisons, correlational analyses for frequency estimates/Nightmare Distress scores), our results suggest that nightmares are associated with altered ReHo in frontal (medial prefrontal and inferior frontal), parietal, temporal and occipital regions, as well as some subcortical regions (thalamus). We also found a positive correlation between retrospective disturbed dreaming frequency estimates and ReHo values in the hippocampus. These findings are mostly in line with a recent SPECT study from our laboratory. Our results point to the possibility that a variety of regions, including but not limited to the limbic-prefrontal circuit of our neurocognitive model, contribute to nightmare formation.
topic nightmares
parasomnias
brain imaging
distress
psychopathology
regional homogeneity
url https://www.frontiersin.org/articles/10.3389/fnins.2021.645255/full
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spelling doaj-bd445acc65bb468782a165f9d77655bb2021-03-18T06:29:00ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2021-03-011510.3389/fnins.2021.645255645255Local Neuronal Synchronization in Frequent Nightmare Recallers and Healthy Controls: A Resting-State Functional Magnetic Resonance Imaging StudyLouis-Philippe Marquis0Louis-Philippe Marquis1Sarah-Hélène Julien2Sarah-Hélène Julien3Véronique Daneault4Véronique Daneault5Cloé Blanchette-Carrière6Cloé Blanchette-Carrière7Tyna Paquette8Michelle Carr9Jean-Paul Soucy10Jacques Montplaisir11Jacques Montplaisir12Tore Nielsen13Tore Nielsen14Department of Psychology, Université de Montréal, Montreal, QC, CanadaCenter for Advanced Research in Sleep Medicine, CIUSSS-NÎM – Hôpital du Sacré-Coeur de Montréal, Montreal, QC, CanadaDepartment of Psychology, Université de Montréal, Montreal, QC, CanadaCenter for Advanced Research in Sleep Medicine, CIUSSS-NÎM – Hôpital du Sacré-Coeur de Montréal, Montreal, QC, CanadaDepartment of Psychology, Université de Montréal, Montreal, QC, CanadaCenter for Advanced Research in Sleep Medicine, CIUSSS-NÎM – Hôpital du Sacré-Coeur de Montréal, Montreal, QC, CanadaDepartment of Psychology, Université de Montréal, Montreal, QC, CanadaCenter for Advanced Research in Sleep Medicine, CIUSSS-NÎM – Hôpital du Sacré-Coeur de Montréal, Montreal, QC, CanadaCenter for Advanced Research in Sleep Medicine, CIUSSS-NÎM – Hôpital du Sacré-Coeur de Montréal, Montreal, QC, CanadaDepartment of Psychiatry, Sleep & Neurophysiology Research Laboratory, University of Rochester Medical Center, Rochester, NY, United StatesMontreal Neurological Institute, Montreal, QC, CanadaCenter for Advanced Research in Sleep Medicine, CIUSSS-NÎM – Hôpital du Sacré-Coeur de Montréal, Montreal, QC, CanadaDepartment of Psychiatry, Université de Montréal, Montreal, QC, CanadaCenter for Advanced Research in Sleep Medicine, CIUSSS-NÎM – Hôpital du Sacré-Coeur de Montréal, Montreal, QC, CanadaDepartment of Psychiatry, Université de Montréal, Montreal, QC, CanadaNightmares are highly dysphoric dreams that are well-remembered upon awakening. Frequent nightmares have been associated with psychopathology and emotional dysregulation, yet their neural mechanisms remain largely unknown. Our neurocognitive model posits that nightmares reflect dysfunction in a limbic-prefrontal circuit comprising medial prefrontal and anterior cingulate cortices, hippocampus, and amygdala. However, there is a paucity of studies that used brain imaging to directly test the neural correlates of nightmares. One such study compared the regional homogeneity (ReHo) of resting-state functional magnetic resonance imaging blood-oxygen level-dependent signals between frequent nightmare recallers and controls. The main results were greater regional homogeneity in the left anterior cingulate cortex and right inferior parietal lobule for the nightmare recallers than for the controls. In the present study, we aimed to document the ReHo correlates of frequent nightmares using several nightmare severity measures. We acquired resting-state functional magnetic resonance imaging data from 18 frequent nightmare recallers aged 18–35 (3 males and 15 females) and 18 age- and sex-matched controls, as well as retrospective and prospective disturbed dreaming frequency estimates and scores on the Nightmare Distress Questionnaire. While there were inconsistent results for our different analyses (group comparisons, correlational analyses for frequency estimates/Nightmare Distress scores), our results suggest that nightmares are associated with altered ReHo in frontal (medial prefrontal and inferior frontal), parietal, temporal and occipital regions, as well as some subcortical regions (thalamus). We also found a positive correlation between retrospective disturbed dreaming frequency estimates and ReHo values in the hippocampus. These findings are mostly in line with a recent SPECT study from our laboratory. Our results point to the possibility that a variety of regions, including but not limited to the limbic-prefrontal circuit of our neurocognitive model, contribute to nightmare formation.https://www.frontiersin.org/articles/10.3389/fnins.2021.645255/fullnightmaresparasomniasbrain imagingdistresspsychopathologyregional homogeneity