Scene unseen: Disrupted neuronal adaptation in melancholia during emotional film viewing

Impairments in attention and concentration are distinctive features of melancholic depression, and may diminish the ability to shift focus away from internal dysphoric states. Disrupted brain networks may underlie the inability to effectively disengage from interoceptive signals in this disorder. Th...

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Main Authors: Matthew P. Hyett, Gordon B. Parker, Christine C. Guo, Andrew Zalesky, Vinh T. Nguyen, Tamara Yuen, Michael Breakspear
Format: Article
Language:English
Published: Elsevier 2015-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158215300115
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spelling doaj-dc02b6fa9f7c4006812d975611a617fb2020-11-25T01:34:35ZengElsevierNeuroImage: Clinical2213-15822015-01-019C66066710.1016/j.nicl.2015.10.011Scene unseen: Disrupted neuronal adaptation in melancholia during emotional film viewingMatthew P. Hyett0Gordon B. Parker1Christine C. Guo2Andrew Zalesky3Vinh T. Nguyen4Tamara Yuen5Michael Breakspear6School of Psychiatry, University of New South Wales, Black Dog Institute Building, Prince of Wales Hospital, Hospital Road, Randwick, NSW 2031, AustraliaSchool of Psychiatry, University of New South Wales, Black Dog Institute Building, Prince of Wales Hospital, Hospital Road, Randwick, NSW 2031, AustraliaQIMR Berghofer Medical Research Institute, 300 Herston Road, Herston, QLD 4006, AustraliaMelbourne Neuropsychiatry Centre, Faculty of Medicine, Dentistry and Health Science & Melbourne School of Engineering, University of Melbourne, VIC 3010, Australia.QIMR Berghofer Medical Research Institute, 300 Herston Road, Herston, QLD 4006, AustraliaSchool of Psychiatry, University of New South Wales, Black Dog Institute Building, Prince of Wales Hospital, Hospital Road, Randwick, NSW 2031, AustraliaQIMR Berghofer Medical Research Institute, 300 Herston Road, Herston, QLD 4006, AustraliaImpairments in attention and concentration are distinctive features of melancholic depression, and may diminish the ability to shift focus away from internal dysphoric states. Disrupted brain networks may underlie the inability to effectively disengage from interoceptive signals in this disorder. This study investigates changes in effective connectivity between cortical systems supporting attention, interoception, and perception in those with melancholic depression when shifting attention from rest to viewing dynamic film stimuli. We hypothesised that those with melancholia would show impaired attentional shifting from rest to emotional film viewing, captured in neuronal states that differed little across conditions. Functional magnetic resonance imaging (fMRI) data were acquired from 48 participants (16 melancholic depressed, 16 non-melancholic depressed, and 16 healthy controls) at rest and whilst viewing emotionally salient movies. Using independent component analysis, we identified 8 cortical modes (default mode, executive control, left/right frontoparietal attention, left/right insula, visual and auditory) and studied their dynamics using dynamic causal modelling. Engagement with dynamic emotional material diminished in melancholia and was associated with network-wide increases in effective connectivity. Melancholia was also characterised by an increase in effective connectivity amongst cortical regions involved in attention and interoception when shifting from rest to negative film viewing, with the converse pattern in control participants. The observed involvement of attention- and insula-based cortical systems highlights a potential neurobiological mechanism for disrupted attentional resource allocation, particularly in switching between interoceptive and exteroceptive signals, in melancholia.http://www.sciencedirect.com/science/article/pii/S2213158215300115AttentionDynamic causal modellingFilm viewingfMRIInteroceptionMelancholic depression
collection DOAJ
language English
format Article
sources DOAJ
author Matthew P. Hyett
Gordon B. Parker
Christine C. Guo
Andrew Zalesky
Vinh T. Nguyen
Tamara Yuen
Michael Breakspear
spellingShingle Matthew P. Hyett
Gordon B. Parker
Christine C. Guo
Andrew Zalesky
Vinh T. Nguyen
Tamara Yuen
Michael Breakspear
Scene unseen: Disrupted neuronal adaptation in melancholia during emotional film viewing
NeuroImage: Clinical
Attention
Dynamic causal modelling
Film viewing
fMRI
Interoception
Melancholic depression
author_facet Matthew P. Hyett
Gordon B. Parker
Christine C. Guo
Andrew Zalesky
Vinh T. Nguyen
Tamara Yuen
Michael Breakspear
author_sort Matthew P. Hyett
title Scene unseen: Disrupted neuronal adaptation in melancholia during emotional film viewing
title_short Scene unseen: Disrupted neuronal adaptation in melancholia during emotional film viewing
title_full Scene unseen: Disrupted neuronal adaptation in melancholia during emotional film viewing
title_fullStr Scene unseen: Disrupted neuronal adaptation in melancholia during emotional film viewing
title_full_unstemmed Scene unseen: Disrupted neuronal adaptation in melancholia during emotional film viewing
title_sort scene unseen: disrupted neuronal adaptation in melancholia during emotional film viewing
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2015-01-01
description Impairments in attention and concentration are distinctive features of melancholic depression, and may diminish the ability to shift focus away from internal dysphoric states. Disrupted brain networks may underlie the inability to effectively disengage from interoceptive signals in this disorder. This study investigates changes in effective connectivity between cortical systems supporting attention, interoception, and perception in those with melancholic depression when shifting attention from rest to viewing dynamic film stimuli. We hypothesised that those with melancholia would show impaired attentional shifting from rest to emotional film viewing, captured in neuronal states that differed little across conditions. Functional magnetic resonance imaging (fMRI) data were acquired from 48 participants (16 melancholic depressed, 16 non-melancholic depressed, and 16 healthy controls) at rest and whilst viewing emotionally salient movies. Using independent component analysis, we identified 8 cortical modes (default mode, executive control, left/right frontoparietal attention, left/right insula, visual and auditory) and studied their dynamics using dynamic causal modelling. Engagement with dynamic emotional material diminished in melancholia and was associated with network-wide increases in effective connectivity. Melancholia was also characterised by an increase in effective connectivity amongst cortical regions involved in attention and interoception when shifting from rest to negative film viewing, with the converse pattern in control participants. The observed involvement of attention- and insula-based cortical systems highlights a potential neurobiological mechanism for disrupted attentional resource allocation, particularly in switching between interoceptive and exteroceptive signals, in melancholia.
topic Attention
Dynamic causal modelling
Film viewing
fMRI
Interoception
Melancholic depression
url http://www.sciencedirect.com/science/article/pii/S2213158215300115
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