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Distinct Aging Effects on Functional Networks in Good and Poor Cognitive Performers

View Article: PubMed Central - PubMed

ABSTRACT

Brain network hubs are susceptible to normal aging processes and disruptions of their functional connectivity are detrimental to decline in cognitive functions in older adults. However, it remains unclear how the functional connectivity of network hubs cope with cognitive heterogeneity in an aging population. This study utilized cognitive and resting-state functional magnetic resonance imaging data, cluster analysis, and graph network analysis to examine age-related alterations in the network hubs’ functional connectivity of good and poor cognitive performers. Our results revealed that poor cognitive performers showed age-dependent disruptions in the functional connectivity of the right insula and posterior cingulate cortex (PCC), while good cognitive performers showed age-related disruptions in the functional connectivity of the left insula and PCC. Additionally, the left PCC had age-related declines in the functional connectivity with the left medial prefrontal cortex (mPFC) and anterior cingulate cortex (ACC). Most interestingly, good cognitive performers showed age-related declines in the functional connectivity of the left insula and PCC with their right homotopic structures. These results may provide insights of neuronal correlates for understanding individual differences in aging. In particular, our study suggests prominent protection roles of the left insula and PCC and bilateral ACC in good performers.

No MeSH data available.


Internetwork connectivity among the salience network (SN), central executive network (CEN), and default mode network (DMN) in poor cognitive performers. Blue color balls indicate hubs identified based on betweenness centrality. Red lines indicate significant age-related decreases in functional connectivity strength, where p < 0.003 after multiple comparison correction. l, left; r, right; SFC, superior frontal cortex; MFC, middle frontal cortex; INS, insula; ACC, anterior cingulate cortex; mPFC, medial prefrontal cortex; PCC, posterior cingulate cortex.
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Figure 3: Internetwork connectivity among the salience network (SN), central executive network (CEN), and default mode network (DMN) in poor cognitive performers. Blue color balls indicate hubs identified based on betweenness centrality. Red lines indicate significant age-related decreases in functional connectivity strength, where p < 0.003 after multiple comparison correction. l, left; r, right; SFC, superior frontal cortex; MFC, middle frontal cortex; INS, insula; ACC, anterior cingulate cortex; mPFC, medial prefrontal cortex; PCC, posterior cingulate cortex.

Mentions: Among the poor cognitive performers, the right insula and bilateral PCC were identified as hubs, indicating their influential roles in the brain functional network. Our analysis further revealed that numerous age-related alterations in the degrees of these hubs, as well as specific hubs-related functional connectivity strength. Specifically, the poor cognitive performers showed significant age-related decreases in the degrees of the right insula and right PCC (p < 0.004; the second column in Table 3). Moreover, the right insula also showed age-related decreases in its functional connectivity with the right ACC in SN (β = -0.358, p = 0.004) and left middle frontal cortex (β = -0.360, p = 0.003) in CEN. The left PCC shows age-related decreases in its functional connectivities with left ACC in the SN (β = -0.396, p = 0.002). The right PCC shows age-related decreases in its functional connectivity with the right middle frontal cortex (β = -0.490, p < 0.001) and right superior frontal cortex (β = -0.556, p < 0.001) in the CEN. The functional connectivity vulnerable to aging is not limited to the hubs’ functional connections. Our results revealed that the functional connectivity between the left superior frontal and left medial prefrontal cortices (β = -0.472, p = 0.001) across the DMN and CEN networks were reduced as age increased. Figure 3 illustrates age effects on these functional connectivities among the SN, DMN, and CEN networks. Coupled with age-related decreases in the functional connectivities with the right insula, the left middle frontal cortex also showed increased betweenness centrality with age (p < 0.001; the third column in Table 3). In addition to the aforementioned findings on the local topological properties of the three functional networks, the poor performers also showed age-related decreases in global and local efficiencies (p < 0.02; Table 4).


Distinct Aging Effects on Functional Networks in Good and Poor Cognitive Performers
Internetwork connectivity among the salience network (SN), central executive network (CEN), and default mode network (DMN) in poor cognitive performers. Blue color balls indicate hubs identified based on betweenness centrality. Red lines indicate significant age-related decreases in functional connectivity strength, where p < 0.003 after multiple comparison correction. l, left; r, right; SFC, superior frontal cortex; MFC, middle frontal cortex; INS, insula; ACC, anterior cingulate cortex; mPFC, medial prefrontal cortex; PCC, posterior cingulate cortex.
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Figure 3: Internetwork connectivity among the salience network (SN), central executive network (CEN), and default mode network (DMN) in poor cognitive performers. Blue color balls indicate hubs identified based on betweenness centrality. Red lines indicate significant age-related decreases in functional connectivity strength, where p < 0.003 after multiple comparison correction. l, left; r, right; SFC, superior frontal cortex; MFC, middle frontal cortex; INS, insula; ACC, anterior cingulate cortex; mPFC, medial prefrontal cortex; PCC, posterior cingulate cortex.
Mentions: Among the poor cognitive performers, the right insula and bilateral PCC were identified as hubs, indicating their influential roles in the brain functional network. Our analysis further revealed that numerous age-related alterations in the degrees of these hubs, as well as specific hubs-related functional connectivity strength. Specifically, the poor cognitive performers showed significant age-related decreases in the degrees of the right insula and right PCC (p < 0.004; the second column in Table 3). Moreover, the right insula also showed age-related decreases in its functional connectivity with the right ACC in SN (β = -0.358, p = 0.004) and left middle frontal cortex (β = -0.360, p = 0.003) in CEN. The left PCC shows age-related decreases in its functional connectivities with left ACC in the SN (β = -0.396, p = 0.002). The right PCC shows age-related decreases in its functional connectivity with the right middle frontal cortex (β = -0.490, p < 0.001) and right superior frontal cortex (β = -0.556, p < 0.001) in the CEN. The functional connectivity vulnerable to aging is not limited to the hubs’ functional connections. Our results revealed that the functional connectivity between the left superior frontal and left medial prefrontal cortices (β = -0.472, p = 0.001) across the DMN and CEN networks were reduced as age increased. Figure 3 illustrates age effects on these functional connectivities among the SN, DMN, and CEN networks. Coupled with age-related decreases in the functional connectivities with the right insula, the left middle frontal cortex also showed increased betweenness centrality with age (p < 0.001; the third column in Table 3). In addition to the aforementioned findings on the local topological properties of the three functional networks, the poor performers also showed age-related decreases in global and local efficiencies (p < 0.02; Table 4).

View Article: PubMed Central - PubMed

ABSTRACT

Brain network hubs are susceptible to normal aging processes and disruptions of their functional connectivity are detrimental to decline in cognitive functions in older adults. However, it remains unclear how the functional connectivity of network hubs cope with cognitive heterogeneity in an aging population. This study utilized cognitive and resting-state functional magnetic resonance imaging data, cluster analysis, and graph network analysis to examine age-related alterations in the network hubs&rsquo; functional connectivity of good and poor cognitive performers. Our results revealed that poor cognitive performers showed age-dependent disruptions in the functional connectivity of the right insula and posterior cingulate cortex (PCC), while good cognitive performers showed age-related disruptions in the functional connectivity of the left insula and PCC. Additionally, the left PCC had age-related declines in the functional connectivity with the left medial prefrontal cortex (mPFC) and anterior cingulate cortex (ACC). Most interestingly, good cognitive performers showed age-related declines in the functional connectivity of the left insula and PCC with their right homotopic structures. These results may provide insights of neuronal correlates for understanding individual differences in aging. In particular, our study suggests prominent protection roles of the left insula and PCC and bilateral ACC in good performers.

No MeSH data available.