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Out-of-sync: disrupted neural activity in emotional circuitry during film viewing in melancholic depression.

Guo CC, Nguyen VT, Hyett MP, Parker GB, Breakspear MJ - Sci Rep (2015)

Bottom Line: We found a marked disengagement of ventromedial prefrontal cortex during natural viewing of a film with negative emotional valence in patients with melancholia.This effect significantly correlated with depression severity.Such changes occurred on the background of diminished consistency of neural activity in visual and auditory sensory networks, as well as higher-order networks involved in emotion and attention, including bilateral intraparietal sulcus and right anterior insula.

View Article: PubMed Central - PubMed

Affiliation: QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.

ABSTRACT
While a rich body of research in controlled experiments has established changes in the neural circuitry of emotion in major depressive disorders, little is known as to how such alterations might translate into complex, naturalistic settings--namely involving dynamic multimodal stimuli with rich contexts, such as those provided by films. Neuroimaging paradigms employing dynamic natural stimuli alleviate the anxiety often associated with complex tasks and eschew the need for laboratory-style abstractions, hence providing an ecologically valid means of elucidating neural underpinnings of neuropsychiatric disorders. To probe the neurobiological signature of refined depression subtypes, we acquired functional neuroimaging data in patients with the melancholic subtype of major depressive disorder during free viewing of emotionally salient films. We found a marked disengagement of ventromedial prefrontal cortex during natural viewing of a film with negative emotional valence in patients with melancholia. This effect significantly correlated with depression severity. Such changes occurred on the background of diminished consistency of neural activity in visual and auditory sensory networks, as well as higher-order networks involved in emotion and attention, including bilateral intraparietal sulcus and right anterior insula. These findings may reflect a failure to re-allocate resources and diminished reactivity to external emotional stimuli in melancholia.

No MeSH data available.


Related in: MedlinePlus

Voxelwise ISC maps in HC and MDD.(A) Group-level ISC maps for HC (left) and MDD (right) during natural viewing of negative, positive and neutral films (p < 0.01, FDR corrected). (B) Group difference maps (MDD < HC) of ISC results for the negative (green) and positive (red) films, and the overlap between the two viewing conditions (yellow; p < 0.05, FDR corrected; cluster size > 50 voxels). Calc = calcarine; dIns = dorsal insula; IFG = inferior frontal gyrus; IPS = intraparietal sulcus; Hes = Heschl’s; mOG = middle occipital gyrus; PCC = posterior cingulate cortex; PCu = precuneus; SMA = supplementary motor area; STG = superior temporal gyrus; vmPFC = ventromedial prefrontal cortex.
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f1: Voxelwise ISC maps in HC and MDD.(A) Group-level ISC maps for HC (left) and MDD (right) during natural viewing of negative, positive and neutral films (p < 0.01, FDR corrected). (B) Group difference maps (MDD < HC) of ISC results for the negative (green) and positive (red) films, and the overlap between the two viewing conditions (yellow; p < 0.05, FDR corrected; cluster size > 50 voxels). Calc = calcarine; dIns = dorsal insula; IFG = inferior frontal gyrus; IPS = intraparietal sulcus; Hes = Heschl’s; mOG = middle occipital gyrus; PCC = posterior cingulate cortex; PCu = precuneus; SMA = supplementary motor area; STG = superior temporal gyrus; vmPFC = ventromedial prefrontal cortex.

Mentions: Free viewing of these films evoked robust and consistent neural activity, as quantified by the inter-subject correlation (ISC) of voxel-wise BOLD signals (Fig 1a, left). Robust inter-subject synchronization in our healthy participants was evident in primary and association visual areas during all three film-viewing conditions. However, consistent responses across more widespread regions were also elicited by the two emotionally salient films, encompassing primary and association auditory cortices, fusiform gyrus (FUS), parahippocampal gyrus (PPA), precuneus (PreC), and supplemental motor area (SMA). These responses extended into higher-order brain regions, including posterior cingulate cortex (PCC), bilateral intraparietal sulcus (IPS), right anterior dorsal insula (dIns) and inferior frontal gyrus (IFG). Notably, the negative film consistently engaged a cluster in the ventromedial prefrontal cortex (vmPFC) in the healthy subjects (Fig. 1a, upper left).


Out-of-sync: disrupted neural activity in emotional circuitry during film viewing in melancholic depression.

Guo CC, Nguyen VT, Hyett MP, Parker GB, Breakspear MJ - Sci Rep (2015)

Voxelwise ISC maps in HC and MDD.(A) Group-level ISC maps for HC (left) and MDD (right) during natural viewing of negative, positive and neutral films (p < 0.01, FDR corrected). (B) Group difference maps (MDD < HC) of ISC results for the negative (green) and positive (red) films, and the overlap between the two viewing conditions (yellow; p < 0.05, FDR corrected; cluster size > 50 voxels). Calc = calcarine; dIns = dorsal insula; IFG = inferior frontal gyrus; IPS = intraparietal sulcus; Hes = Heschl’s; mOG = middle occipital gyrus; PCC = posterior cingulate cortex; PCu = precuneus; SMA = supplementary motor area; STG = superior temporal gyrus; vmPFC = ventromedial prefrontal cortex.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4481375&req=5

f1: Voxelwise ISC maps in HC and MDD.(A) Group-level ISC maps for HC (left) and MDD (right) during natural viewing of negative, positive and neutral films (p < 0.01, FDR corrected). (B) Group difference maps (MDD < HC) of ISC results for the negative (green) and positive (red) films, and the overlap between the two viewing conditions (yellow; p < 0.05, FDR corrected; cluster size > 50 voxels). Calc = calcarine; dIns = dorsal insula; IFG = inferior frontal gyrus; IPS = intraparietal sulcus; Hes = Heschl’s; mOG = middle occipital gyrus; PCC = posterior cingulate cortex; PCu = precuneus; SMA = supplementary motor area; STG = superior temporal gyrus; vmPFC = ventromedial prefrontal cortex.
Mentions: Free viewing of these films evoked robust and consistent neural activity, as quantified by the inter-subject correlation (ISC) of voxel-wise BOLD signals (Fig 1a, left). Robust inter-subject synchronization in our healthy participants was evident in primary and association visual areas during all three film-viewing conditions. However, consistent responses across more widespread regions were also elicited by the two emotionally salient films, encompassing primary and association auditory cortices, fusiform gyrus (FUS), parahippocampal gyrus (PPA), precuneus (PreC), and supplemental motor area (SMA). These responses extended into higher-order brain regions, including posterior cingulate cortex (PCC), bilateral intraparietal sulcus (IPS), right anterior dorsal insula (dIns) and inferior frontal gyrus (IFG). Notably, the negative film consistently engaged a cluster in the ventromedial prefrontal cortex (vmPFC) in the healthy subjects (Fig. 1a, upper left).

Bottom Line: We found a marked disengagement of ventromedial prefrontal cortex during natural viewing of a film with negative emotional valence in patients with melancholia.This effect significantly correlated with depression severity.Such changes occurred on the background of diminished consistency of neural activity in visual and auditory sensory networks, as well as higher-order networks involved in emotion and attention, including bilateral intraparietal sulcus and right anterior insula.

View Article: PubMed Central - PubMed

Affiliation: QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.

ABSTRACT
While a rich body of research in controlled experiments has established changes in the neural circuitry of emotion in major depressive disorders, little is known as to how such alterations might translate into complex, naturalistic settings--namely involving dynamic multimodal stimuli with rich contexts, such as those provided by films. Neuroimaging paradigms employing dynamic natural stimuli alleviate the anxiety often associated with complex tasks and eschew the need for laboratory-style abstractions, hence providing an ecologically valid means of elucidating neural underpinnings of neuropsychiatric disorders. To probe the neurobiological signature of refined depression subtypes, we acquired functional neuroimaging data in patients with the melancholic subtype of major depressive disorder during free viewing of emotionally salient films. We found a marked disengagement of ventromedial prefrontal cortex during natural viewing of a film with negative emotional valence in patients with melancholia. This effect significantly correlated with depression severity. Such changes occurred on the background of diminished consistency of neural activity in visual and auditory sensory networks, as well as higher-order networks involved in emotion and attention, including bilateral intraparietal sulcus and right anterior insula. These findings may reflect a failure to re-allocate resources and diminished reactivity to external emotional stimuli in melancholia.

No MeSH data available.


Related in: MedlinePlus