Age- and Sex-Related Topological Organization of Human Brain Functional Networks and Their Relationship to Cognition

Foo, Heidi; Thalamuthu, Anbupalam; Jiang, Jiyang; Koch, Forrest; Mather, Karen A.; Wang, Wen; Sachdev, Perminder S.

doi:10.3389/fnagi.2021.758817

Cited by 15 publications

(18 citation statements)

References 60 publications

(85 reference statements)

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“…These findings agree with results from previous studies showing different functional trajectories between men and women [16, 55]. However, in contrast to previous studies, here we demonstrate that, although the functional connectomes of younger men and women are different, they become increasingly similar with older age possibly due to a faster rate of functional changes observed in the brains of men [48], which is in line with studies showing that men have lower resilience to age-related cognitive decline compared to women [22].…”

Section: Discussionsupporting

confidence: 91%

“…In combination with large samples, these measures can improve our understanding of brain connectivity [25], and, in particular, our ability to predict sex differences over the course of aging [45]. Previous studies of brain connectivity and network topology have mainly focused on measures that exclude the negative connections or average the effects of positive and negative connections [13,23,[46][47][48]. However, changes in the interaction between positive and negative connectivity could be a more sensitive marker of abnormalities that occur in men and women in middle and late adulthood.…”

Section: Discussionmentioning

confidence: 99%

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Sex differences in functional network topology over the course of aging in 37543 UK Biobank participants

Mijalkov

Veréb

Jamialahmadi

et al. 2022

Preprint

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Aging is a major risk factor for cardiovascular and neurodegenerative disorders, with considerable societal and economic implications. Healthy aging is accompanied by changes in connectivity between and within resting-state functional networks, however, there is no consensus on the impact of sex on these age-related alterations. Here, in a large cross-sectional sample of 37543 UK Biobank participants, we show that multilayer measures that capture the interaction between positive and negative connections provide crucial information on the impact of sex on age-related changes in network topology, being closely related to cognitive, structural, and cardiovascular risk factors that have been shown to differ between men and women. We also provide additional insights into the genetic influences on multilayer connectivity changes that occur during aging. Our findings indicate that multilayer measures contain previously unknown information on the relationship between sex and age, opening up new avenues for research into functional brain connectivity in aging.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Sex differences in functional network topology over the course of aging in 37543 UK Biobank participants

Mijalkov

Veréb

Jamialahmadi

et al. 2022

Preprint

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“…Soch et al, 2021b, Fig. 2; also see Maillet and Rajah, 2014; Billette et al, in review); (iii) resting-state fMRI patterns exhibit global age-related differences (Foo et al, 2021; Xing, 2021), and (iv) quantitative structural MRI approaches like VBM yield robust and well-replicated age-related differences, with older adults showing reduced hippocampal volumes (cf. Kizilirmak et al, in prep., Fig.…”

Section: Discussionmentioning

confidence: 99%

“…In the present study, we have comparatively evaluated the ability of structural and functional (resting-state and task-based) MRI data as well as behavioral measures to predict chronological age versus memory performance in young and older healthy adults (see Figure 1). (Foo et al, 2021;Xing, 2021), and (iv) quantitative structural MRI approaches like VBM yield robust and well-replicated age-related differences, with older adults showing reduced hippocampal volumes (cf. Kizilirmak et al,in prep.,Fig.…”

Section: Discussionmentioning

confidence: 99%

Structural and functional MRI data differentially predict chronological age and behavioral memory performance

Soch

Richter

Kizilirmak

et al. 2022

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Human cognitive abilities decline with increasing chronological age, with decreased explicit memory performance being most strongly affected. However, some older adults show "successful aging", that is, relatively preserved cognitive ability in old age. One explanation for this could be higher brain structural integrity in these individuals. Alternatively, the brain might recruit existing resources more efficiently or employ compensatory cognitive strategies. Here, we approached this question by testing multiple candidate variables from structural and functional neuroimaging for their ability to predict chronological age and memory performance, respectively. Prediction was performed using support vector machine (SVM) classification and regression across and within two samples of young (N = 106) and older (N = 153) adults. The candidate variables were (i) behavioral response frequencies in an episodic memory test, (ii) recently described fMRI scores reflecting preservation of functional memory networks, (iii) whole-brain fMRI contrasts for novelty processing and subsequent memory, (iv) resting-state fMRI maps quantifying voxel-wise signal fluctuation and (v) gray matter volume estimated from structural MR images. While age group could be reliably decoded from all variables, chronological age within young and older subjects was best predicted from gray matter volume. In contrast, memory performance was best predicted from task-based fMRI contrasts and particularly single-value fMRI scores, whereas gray matter volume has no predictive power with respect to memory performance in healthy adults. Our results suggest that superior memory performance in healthy older adults is better explained by efficient recruitment of memory networks rather than by preserved brain structure.

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“…Advanced age is associated with an overall decrease in the effectiveness of specialized communication at the global network level (ie, integration) and loss of functional specialization at the local level of specific brain regions (ie, segregation). That is, neuronal networks become less distinct with advanced age (1).…”

Section: Introductionmentioning

confidence: 99%

Network Segregation in Aging Females and Evaluation of the Impact of Sex Steroid Hormones

Hicks¹,

Magalhães²,

Ballard³

et al. 2022

Preprint

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Males and females show differential patterns in connectivity in resting-state networks (RSNs) during normal aging, from early adulthood to late middle age. Age-related differences in network integration (effectiveness of specialized communication at the global network level) and segregation (functional specialization at the local level of specific brain regions) may also differ by sex. These differences may be due at least in part to endogenous hormonal fluctuation, such as that which occurs in females during midlife with the transition to menopause when levels of estrogens and progesterone drop markedly. A limited number of studies that have investigated sex differences in the action of steroid hormones in brain networks. Here we investigated how sex steroid hormones relate to age-network relationships in both males and females, with a focus on network segregation. Females displayed a significant quadratic relationship between age and network segregation for the cerebellar-basal ganglia and salience networks. In both cases, segregation was still increasing through adulthood, highest in midlife, and with a downturn thereafter. However, there were no significant relationships between sex steroid hormone levels and network segregation levels in females, and they did not exhibit significant associations between progesterone or 17β-estradiol and network segregation. Patterns of connectivity between the cerebellum and basal ganglia have been associated with cognitive performance and self-reported balance confidence in older adults. Together, these findings suggest that network segregation patterns with age in females vary by network, and that sex steroid hormones are not associated with this measure of connectivity in this cross-sectional analysis. Though this is a null effect, it remains critical for understanding the extent to which hormones relate to brain network architecture.

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Age- and Sex-Related Topological Organization of Human Brain Functional Networks and Their Relationship to Cognition

Cited by 15 publications

References 60 publications

Sex differences in functional network topology over the course of aging in 37543 UK Biobank participants

Sex differences in functional network topology over the course of aging in 37543 UK Biobank participants

Structural and functional MRI data differentially predict chronological age and behavioral memory performance

Network Segregation in Aging Females and Evaluation of the Impact of Sex Steroid Hormones

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