Small vessel disease and cognitive impairment: The relevance of central network connections

Reijmer, Yaël D.; Fotiadis, Panagiotis; Piantoni, Giovanni; Boulouis, Grégoire; Kelly, Kathleen; Gurol, M. Edip; Leemans, Alexander; O’Sullivan, Michael; Greenberg, Steven M.; Viswanathan, Anand

doi:10.1002/hbm.23186

Cited by 43 publications

(44 citation statements)

References 39 publications

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“…The association between the rich club connection strength and cognitive impairment provides evidence for a possible link between the rich club (dis)organisation and the occurrence of cognitive impairment in symptomatic SVD. This is further corroborated by a recent study showing that central network connections, which were based on edge betweenness centrality, were related to cognitive impairment in SVD [Reijmer et al, 2016]. Although network centrality does not directly measure rich club organisation, the connections in the rich club are likely to be among the most central suggesting these independent findings provide convergent evidence.…”

Section: Figuresupporting

confidence: 75%

Disruption of rich club organisation in cerebral small vessel disease

Tuladhar

Lawrence

Norris

et al. 2016

Human Brain Mapping

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Cerebral small vessel disease (SVD) is an important cause of vascular cognitive impairment. Recent studies have demonstrated that structural connectivity of brain networks in SVD is disrupted. However, little is known about the extent and location of the reduced connectivity in SVD. Here they investigate the rich club organisation-a set of highly connected and interconnected regions-and investigate whether there is preferential rich club disruption in SVD. Diffusion tensor imaging (DTI) and cognitive assessment were performed in a discovery sample of SVD patients (n 5 115) and healthy control subjects (n 5 50). Results were replicated in an independent dataset (49 SVD with confluent WMH cases and 108 SVD controls) with SVD patients having a similar SVD phenotype to that of the discovery cases. Rich club organisation was examined in structural networks derived from DTI followed by deterministic tractography. Structural networks in SVD patients were less dense with lower network strength and efficiency. Reduced connectivity was found in SVD, which was preferentially This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. located in the connectivity between the rich club nodes rather than in the feeder and peripheral connections, a finding confirmed in both datasets. In discovery dataset, lower rich club connectivity was associated with lower scores on psychomotor speed (b 5 0.29, P < 0.001) and executive functions (b 5 0.20, P 5 0.009). These results suggest that SVD is characterized by abnormal connectivity between rich club hubs in SVD and provide evidence that abnormal rich club organisation might contribute to the development of cognitive impairment in SVD.

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Section: Figuresupporting

confidence: 75%

Disruption of rich club organisation in cerebral small vessel disease

Tuladhar

Lawrence

Norris

et al. 2016

Human Brain Mapping

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“…Previous work has indeed demonstrated the relevance of connections with high network centrality to global efficiency and executive functioning in patients with small vessel disease. 19 …”

Section: Discussionmentioning

confidence: 99%

“…18 White matter hyperintensity (WMH) volume was calculated using an automated method based on thresholding the segmented white matter FLAIR intensity maps (see for more detail 19 ). All the results generated by this algorithm were manually checked to verify their accuracy.…”

Section: Methodsmentioning

confidence: 99%

Progression of Brain Network Alterations in Cerebral Amyloid Angiopathy

Reijmer

Fotiadis

Riley

et al. 2016

Stroke

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Background and Purpose We recently showed that cerebral amyloid angiopathy (CAA) is associated with functionally relevant brain network impairments, in particular affecting posterior white matter connections. Here we examined how these brain network impairments progress over time. Methods Thirty-three patients with probable CAA underwent multimodal brain MRI at two time points (mean follow-up time: 1.3±0.4 years). Brain networks of the hemisphere free of intracerebral hemorrhages were reconstructed using fiber tractography and graph theory. The global efficiency of the network and mean fractional anisotropies (FA) of posterior-posterior, frontal-frontal, and posterior-frontal network connections were calculated. Patients with moderate vs. severe CAA were defined based on microbleed count, dichotomized at the median (median=35). Results Global efficiency of the ICH-free hemispheric network declined from baseline to follow up (−0.008 ± 0.003, p=0.029). The decline in global efficiency was most pronounced for patients with severe CAA (group × time interaction p=0.03). The decline in global network efficiency was associated with worse executive functioning (Beta=0.46, p=0.03). Examination of subgroups of network connections revealed a decline in FA of posterior-posterior connections at both levels of CAA severity (−0.006 ± 0.002, p=0.017; group × time interaction p=0.16). The FA of posterior-frontal and frontal-frontal connections declined in patients with severe but not moderate CAA (group × time interaction: p=0.007 and p=0.005). Associations were independent of change in white matter hyperintensity volume. Conclusions Brain network impairment in patients with CAA worsens measurably over just 1.3-year follow-up and appear to progress from posterior to frontal connections with increasing disease severity.

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“…In this study, we assume the existence of a central subnetwork that is shared across participants (Reijmer et al, ). To identify this central subnetwork, the average brain network across both patients and controls was determined by including those connections which occurred in more than two‐thirds of the participants (de Reus and van den Heuvel, ).…”

Section: Methodsmentioning

confidence: 99%

Central and non‐central networks, cognition, clinical symptoms, and polygenic risk scores in schizophrenia

Alloza

Bastin

Cox

et al. 2017

Human Brain Mapping

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Schizophrenia is a complex disorder that may be the result of aberrant connections between specific brain regions rather than focal brain abnormalities. Here, we investigate the relationships between brain structural connectivity as described by network analysis, intelligence, symptoms, and polygenic risk scores (PGRS) for schizophrenia in a group of patients with schizophrenia and a group of healthy controls. Recently, researchers have shown an interest in the role of high centrality networks in the disorder. However, the importance of non‐central networks still remains unclear. Thus, we specifically examined network‐averaged fractional anisotropy (mean edge weight) in central and non‐central subnetworks. Connections with the highest betweenness centrality within the average network (>75% of centrality values) were selected to represent the central subnetwork. The remaining connections were assigned to the non‐central subnetwork. Additionally, we calculated graph theory measures from the average network (connections that occur in at least 2/3 of participants). Density, strength, global efficiency, and clustering coefficient were significantly lower in patients compared with healthy controls for the average network (pFDR < 0.05). All metrics across networks were significantly associated with intelligence (pFDR < 0.05). There was a tendency towards significance for a correlation between intelligence and PGRS for schizophrenia (r = −0.508, p = 0.052) that was significantly mediated by central and non‐central mean edge weight and every graph metric from the average network. These results are consistent with the hypothesis that intelligence deficits are associated with a genetic risk for schizophrenia, which is mediated via the disruption of distributed brain networks. Hum Brain Mapp 38:5919–5930, 2017. © 2017 Wiley Periodicals, Inc.

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Small vessel disease and cognitive impairment: The relevance of central network connections

Cited by 43 publications

References 39 publications

Disruption of rich club organisation in cerebral small vessel disease

Disruption of rich club organisation in cerebral small vessel disease

Progression of Brain Network Alterations in Cerebral Amyloid Angiopathy

Central and non‐central networks, cognition, clinical symptoms, and polygenic risk scores in schizophrenia

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