Hyperconnectivity and altered interactions of a nucleus accumbens network in post-stroke depression

Lena K.L. Oestreich; Paul Wright; Michael J. O'sullivan

doi:10.1093/braincomms/fcac281

Hyperconnectivity and altered interactions of a nucleus accumbens network in post-stroke depression

Lena K.L. Oestreich^*, Paul Wright, Michael J. O'sullivan

^*Corresponding author for this work

Biomedical Engineering Department

Research output: Contribution to journal › Article › peer-review

6 Citations (Scopus)

Abstract

Post-stroke depression is a common complication of stroke. To date, no consistent locus of injury is associated with this complication. Here, we probed network dynamics and structural alterations in post-stroke depression in four functional circuits linked to major depressive disorder and a visual network, which served as a control network. Forty-four participants with recent stroke (mean age = 69.03, standard deviation age = 8.59, age range = 51-86 and gender: female = 10) and 16 healthy volunteers (mean age = 71.53, standard deviation age = 10.62, age range = 51-84 and gender: female = 11) were imaged with 3-Tesla structural, diffusion and resting-state functional MRI. The Geriatric Depression Scale was administered to measure depression severity. Associations between depression severity and functional connectivity were investigated within networks seeded from nucleus accumbens, amygdala, dorsolateral prefrontal cortex and primary visual cortex. In addition, the default mode network was identified by connectivity with medial prefrontal cortex and posterior cingulate cortex. Circuits that exhibited altered activity associated with depression severity were further investigated by extracting within-network volumetric and microstructural measures from structural images. In the stroke group, functional connectivity within the nucleus accumbens-seeded network (left hemisphere: P = 0.001; and right hemisphere: P = 0.004) and default mode network (cluster one: P < 0.001; and cluster two: P < 0.001) correlated positively with depressive symptoms. Normal anticorrelations between these two networks were absent in patients with post-stroke depression. Grey matter volume of the right posterior cingulate cortex (Pearson correlation coefficient = -0.286, P = 0.03), as well as microstructural measures in the posterior cingulate cortex (right: Pearson correlation coefficient = 0.4, P = 0.024; and left: Pearson correlation coefficient = 0.3, P = 0.048), right medial prefrontal cortex (Pearson correlation coefficient = 0.312, P = 0.039) and the medial forebrain bundle (Pearson correlation coefficient = 0.450, P = 0.003), a major projection pathway interconnecting the nucleus accumbens-seeded network and linking to medial prefrontal cortex, were associated with depression severity. Depression after stroke is marked by reduced mutual inhibition between functional circuits involving nucleus accumbens and default mode network as well as volumetric and microstructural changes within these networks. Aberrant network dynamics present in patients with post-stroke depression are therefore likely to be influenced by secondary, pervasive alterations in grey and white matter, remote from the site of injury.

Original language	English
Article number	fcac281
Journal	Brain Communications
Volume	4
Issue number	6
DOIs	https://doi.org/10.1093/braincomms/fcac281
Publication status	Published - 2 Nov 2022

Keywords

default mode network (DMN)
diffusion MRI
post-stroke depression
resting-state functional MRI
stroke

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1093/braincomms/fcac281

Cite this

@article{19a6d13c506444ecb58b845d89458a84,

title = "Hyperconnectivity and altered interactions of a nucleus accumbens network in post-stroke depression",

abstract = "Post-stroke depression is a common complication of stroke. To date, no consistent locus of injury is associated with this complication. Here, we probed network dynamics and structural alterations in post-stroke depression in four functional circuits linked to major depressive disorder and a visual network, which served as a control network. Forty-four participants with recent stroke (mean age = 69.03, standard deviation age = 8.59, age range = 51-86 and gender: female = 10) and 16 healthy volunteers (mean age = 71.53, standard deviation age = 10.62, age range = 51-84 and gender: female = 11) were imaged with 3-Tesla structural, diffusion and resting-state functional MRI. The Geriatric Depression Scale was administered to measure depression severity. Associations between depression severity and functional connectivity were investigated within networks seeded from nucleus accumbens, amygdala, dorsolateral prefrontal cortex and primary visual cortex. In addition, the default mode network was identified by connectivity with medial prefrontal cortex and posterior cingulate cortex. Circuits that exhibited altered activity associated with depression severity were further investigated by extracting within-network volumetric and microstructural measures from structural images. In the stroke group, functional connectivity within the nucleus accumbens-seeded network (left hemisphere: P = 0.001; and right hemisphere: P = 0.004) and default mode network (cluster one: P < 0.001; and cluster two: P < 0.001) correlated positively with depressive symptoms. Normal anticorrelations between these two networks were absent in patients with post-stroke depression. Grey matter volume of the right posterior cingulate cortex (Pearson correlation coefficient = -0.286, P = 0.03), as well as microstructural measures in the posterior cingulate cortex (right: Pearson correlation coefficient = 0.4, P = 0.024; and left: Pearson correlation coefficient = 0.3, P = 0.048), right medial prefrontal cortex (Pearson correlation coefficient = 0.312, P = 0.039) and the medial forebrain bundle (Pearson correlation coefficient = 0.450, P = 0.003), a major projection pathway interconnecting the nucleus accumbens-seeded network and linking to medial prefrontal cortex, were associated with depression severity. Depression after stroke is marked by reduced mutual inhibition between functional circuits involving nucleus accumbens and default mode network as well as volumetric and microstructural changes within these networks. Aberrant network dynamics present in patients with post-stroke depression are therefore likely to be influenced by secondary, pervasive alterations in grey and white matter, remote from the site of injury.",

keywords = "default mode network (DMN), diffusion MRI, post-stroke depression, resting-state functional MRI, stroke",

author = "Oestreich, {Lena K.L.} and Paul Wright and O'sullivan, {Michael J.}",

note = "Funding Information: This study was supported by the Medical Research Council, UK (grant reference MR/K022113/1), the European Commission Horizon 2020 Health Programme (CoSTREAM, grant agreement 667375) and a National Health and Medical Research Council (NHMRC) Investigator Grant (2021/GNT2007718) to Lena Oestreich. Publisher Copyright: {\textcopyright} 2022 The Author(s).",

year = "2022",

month = nov,

day = "2",

doi = "10.1093/braincomms/fcac281",

language = "English",

volume = "4",

journal = "Brain Communications",

issn = "2632-1297",

publisher = "Oxford University Press",

number = "6",

}

TY - JOUR

T1 - Hyperconnectivity and altered interactions of a nucleus accumbens network in post-stroke depression

AU - Oestreich, Lena K.L.

AU - Wright, Paul

AU - O'sullivan, Michael J.

N1 - Funding Information: This study was supported by the Medical Research Council, UK (grant reference MR/K022113/1), the European Commission Horizon 2020 Health Programme (CoSTREAM, grant agreement 667375) and a National Health and Medical Research Council (NHMRC) Investigator Grant (2021/GNT2007718) to Lena Oestreich. Publisher Copyright: © 2022 The Author(s).

PY - 2022/11/2

Y1 - 2022/11/2

N2 - Post-stroke depression is a common complication of stroke. To date, no consistent locus of injury is associated with this complication. Here, we probed network dynamics and structural alterations in post-stroke depression in four functional circuits linked to major depressive disorder and a visual network, which served as a control network. Forty-four participants with recent stroke (mean age = 69.03, standard deviation age = 8.59, age range = 51-86 and gender: female = 10) and 16 healthy volunteers (mean age = 71.53, standard deviation age = 10.62, age range = 51-84 and gender: female = 11) were imaged with 3-Tesla structural, diffusion and resting-state functional MRI. The Geriatric Depression Scale was administered to measure depression severity. Associations between depression severity and functional connectivity were investigated within networks seeded from nucleus accumbens, amygdala, dorsolateral prefrontal cortex and primary visual cortex. In addition, the default mode network was identified by connectivity with medial prefrontal cortex and posterior cingulate cortex. Circuits that exhibited altered activity associated with depression severity were further investigated by extracting within-network volumetric and microstructural measures from structural images. In the stroke group, functional connectivity within the nucleus accumbens-seeded network (left hemisphere: P = 0.001; and right hemisphere: P = 0.004) and default mode network (cluster one: P < 0.001; and cluster two: P < 0.001) correlated positively with depressive symptoms. Normal anticorrelations between these two networks were absent in patients with post-stroke depression. Grey matter volume of the right posterior cingulate cortex (Pearson correlation coefficient = -0.286, P = 0.03), as well as microstructural measures in the posterior cingulate cortex (right: Pearson correlation coefficient = 0.4, P = 0.024; and left: Pearson correlation coefficient = 0.3, P = 0.048), right medial prefrontal cortex (Pearson correlation coefficient = 0.312, P = 0.039) and the medial forebrain bundle (Pearson correlation coefficient = 0.450, P = 0.003), a major projection pathway interconnecting the nucleus accumbens-seeded network and linking to medial prefrontal cortex, were associated with depression severity. Depression after stroke is marked by reduced mutual inhibition between functional circuits involving nucleus accumbens and default mode network as well as volumetric and microstructural changes within these networks. Aberrant network dynamics present in patients with post-stroke depression are therefore likely to be influenced by secondary, pervasive alterations in grey and white matter, remote from the site of injury.

AB - Post-stroke depression is a common complication of stroke. To date, no consistent locus of injury is associated with this complication. Here, we probed network dynamics and structural alterations in post-stroke depression in four functional circuits linked to major depressive disorder and a visual network, which served as a control network. Forty-four participants with recent stroke (mean age = 69.03, standard deviation age = 8.59, age range = 51-86 and gender: female = 10) and 16 healthy volunteers (mean age = 71.53, standard deviation age = 10.62, age range = 51-84 and gender: female = 11) were imaged with 3-Tesla structural, diffusion and resting-state functional MRI. The Geriatric Depression Scale was administered to measure depression severity. Associations between depression severity and functional connectivity were investigated within networks seeded from nucleus accumbens, amygdala, dorsolateral prefrontal cortex and primary visual cortex. In addition, the default mode network was identified by connectivity with medial prefrontal cortex and posterior cingulate cortex. Circuits that exhibited altered activity associated with depression severity were further investigated by extracting within-network volumetric and microstructural measures from structural images. In the stroke group, functional connectivity within the nucleus accumbens-seeded network (left hemisphere: P = 0.001; and right hemisphere: P = 0.004) and default mode network (cluster one: P < 0.001; and cluster two: P < 0.001) correlated positively with depressive symptoms. Normal anticorrelations between these two networks were absent in patients with post-stroke depression. Grey matter volume of the right posterior cingulate cortex (Pearson correlation coefficient = -0.286, P = 0.03), as well as microstructural measures in the posterior cingulate cortex (right: Pearson correlation coefficient = 0.4, P = 0.024; and left: Pearson correlation coefficient = 0.3, P = 0.048), right medial prefrontal cortex (Pearson correlation coefficient = 0.312, P = 0.039) and the medial forebrain bundle (Pearson correlation coefficient = 0.450, P = 0.003), a major projection pathway interconnecting the nucleus accumbens-seeded network and linking to medial prefrontal cortex, were associated with depression severity. Depression after stroke is marked by reduced mutual inhibition between functional circuits involving nucleus accumbens and default mode network as well as volumetric and microstructural changes within these networks. Aberrant network dynamics present in patients with post-stroke depression are therefore likely to be influenced by secondary, pervasive alterations in grey and white matter, remote from the site of injury.

KW - default mode network (DMN)

KW - diffusion MRI

KW - post-stroke depression

KW - resting-state functional MRI

KW - stroke

UR - http://www.scopus.com/inward/record.url?scp=85144541355&partnerID=8YFLogxK

U2 - 10.1093/braincomms/fcac281

DO - 10.1093/braincomms/fcac281

M3 - Article

AN - SCOPUS:85144541355

SN - 2632-1297

VL - 4

JO - Brain Communications

JF - Brain Communications

IS - 6

M1 - fcac281

ER -

Hyperconnectivity and altered interactions of a nucleus accumbens network in post-stroke depression

Abstract

Keywords

UN SDGs

Access to Document

Other files and links

Fingerprint

Cite this