Converging evidence of impaired brain function in systemic lupus erythematosus: changes in perfusion dynamics and intrinsic functional connectivity

Papadaki, Efrosini; Simos, Nicholas J; Kavroulakis, Eleftherios; Βertsias, George; Antypa, Despina; Fanouriakis, Antonis; Maris, Thomas G.; Sidiropoulos, Prodromos; Boumpas, Dimitrios T.

doi:10.1007/s00234-022-02924-x

Cited by 7 publications

(17 citation statements)

References 39 publications

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“…Other clinical applications include the detection of perfusion deficits in Alzheimer's disease that confirmed the rsfMRI signal delay in the bilateral precuneus, which is consistent with previous ASL studies showing hypoperfusion patterns in these areas 93 . In a study evaluating the relationships between the rsfMRI time lag, functional connectivity, and cognitive performance in neuropsychiatric systemic lupus erythematosus, the rsfMRI signal was more delayed in the patient group than in healthy control group and the delay in the cingulate cortex was significantly associated with neuropsychological test scores 94 . Studies on patients with temporal lobe epilepsy have shown that the rsfMRI signal was delayed in the temporal lobe on the side of involvement 95,96 .…”

Section: Clinical Applications Of Rsfmri Global Signal Metricssupporting

confidence: 89%

“…93 In a study evaluating the relationships between the rsfMRI time lag, functional connectivity, and 90 cognitive performance in neuropsychiatric systemic lupus erythematosus, the rsfMRI signal was more delayed in the patient group than in healthy control group and the delay in the cingulate cortex was significantly associated with neuropsychological test scores. 94 Studies on patients with temporal lobe epilepsy have shown that the rsfMRI signal was delayed in the temporal lobe on the side of involvement. 95,96 One study incorporated the rsfMRI time delay into a connectivity analysis, showing that the interhemispheric correlation metrics were significantly lower in a group of patients with unfavorable surgical outcomes.…”

Section: Clinical Applications Of Rsfmri Global Signal Metricsmentioning

confidence: 99%

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Resting‐State fMRI: Emerging Concepts for Future Clinical Application

Amemiya

Takao

Abe

2023

Magnetic Resonance Imaging

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Resting‐state functional magnetic resonance imaging (rsfMRI) has been developed as a method of investigating spontaneous neural activity. Based on its low‐frequency signal synchronization, rsfMRI has made it possible to identify multiple macroscopic structures termed resting‐state networks (RSNs) on a single scan of less than 10 minutes. It is easy to implement even in clinical practice, in which assigning tasks to patients can be challenging. These advantages have accelerated the adoption and growth of rsfMRI. Recently, studies on the global rsfMRI signal have attracted increasing attention. Because it primarily arises from physiological events, less attention has hitherto been paid to the global signal than to the local network (i.e., RSN) component. However, the global signal is not a mere nuisance or a subsidiary component. On the contrary, it is quantitatively the dominant component that accounts for most of the variance in the rsfMRI signal throughout the brain and provides rich information on local hemodynamics that can serve as an individual‐level diagnostic biomarker. Moreover, spatiotemporal analyses of the global signal have revealed that it is closely and fundamentally associated with the organization of RSNs, thus challenging the basic assumptions made in conventional rsfMRI analyses and views on RSNs. This review introduces new concepts emerging from rsfMRI spatiotemporal analyses focusing on the global signal and discusses how they may contribute to future clinical medicine.Evidence Level5Technical EfficacyStage 1

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Section: Clinical Applications Of Rsfmri Global Signal Metricssupporting

confidence: 89%

Section: Clinical Applications Of Rsfmri Global Signal Metricsmentioning

confidence: 99%

Resting‐State fMRI: Emerging Concepts for Future Clinical Application

Amemiya

Takao

Abe

2023

Magnetic Resonance Imaging

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“…Regarding SPL, hyperconnectivity was accompanied by reduced cortical volume (in the right hemisphere) in agreement with results from an independent sample of patients with NPSLE 7 and by increased haemodynamic lag (bilaterally) in the current cohort of patients with NPSLE. 11 Hyperconnectivity of the left angular gyrus was observed in patients with NPSLE and patients without NPSLE as a robust finding, given that it was supported by three complementary measures of BOLD signal interdependency (derived from CRQA) and was also evident on static FC analyses (derived from Pearson correlation metrics 11 ). In general, these results are consistent with growing evidence that patients without NPSLE may also display functional brain alterations, although generally milder than those found in patients with NPSLE.…”

Section: Parietal Hyperconnectivity In Npslementioning

confidence: 93%

“…In the earliest attempt to assess FC in patients with NPSLE, Nystedt et al reported both reduced and increased FC in patients with NPSLE as compared with healthy controls (HCs) within several, a priori-defined networks. 9 10 Our group has applied wholebrain FC network modelling techniques, [11][12][13] targeting individual variability in FC network structure, in the presence of largely unknown anatomical and haemodynamic alterations in a highly heterogeneous disease. According to these studies, patients with NPSLE displayed increased nodal connectivity, as compared with age-matched volunteer HCs, indexed through Intrinsic Connectivity Contrast (ICC), in the superior parietal lobule bilaterally (SPL and precuneus) and in the left angular gyrus.…”

Section: How This Study Might Affect Research Practice or Policymentioning

confidence: 99%

Altered hippocampal connectivity dynamics predicts memory performance in neuropsychiatric lupus: a resting-state fMRI study using cross-recurrence quantification analysis

et al. 2023

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ObjectiveΤo determine whole-brain and regional functional connectivity (FC) characteristics of patients with neuropsychiatric SLE (NPSLE) or without neuropsychiatric manifestations (non-NPSLE) and examine their association with cognitive performance.MethodsCross-recurrence quantification analysis (CRQA) of resting-state functional MRI (rs-fMRI) data was performed in 44 patients with NPSLE, 20 patients without NPSLE and 35 healthy controls (HCs). Volumetric analysis of total brain and specific cortical and subcortical regions, where significant connectivity changes were identified, was performed. Cognitive status of patients with NPSLE was assessed by neuropsychological tests. Group comparisons on nodal FC, global network metrics and regional volumetrics were conducted, and associations with cognitive performance were estimated (at p<0.05 false discovery rate corrected).ResultsFC in patients with NPSLE was characterised by increased modularity (mean (SD)=0.31 (0.06)) as compared with HCs (mean (SD)=0.27 (0.06); p=0.05), hypoconnectivity of the left (mean (SD)=0.06 (0.018)) and right hippocampi (mean (SD)=0.051 (0.0.16)), and of the right amygdala (mean (SD)=0.091 (0.039)), as compared with HCs (mean (SD)=0.075 (0.022), p=0.02; 0.065 (0.019), p=0.01; 0.14 (0.096), p=0.05, respectively). Hyperconnectivity of the left angular gyrus (NPSLE/HCs: mean (SD)=0.29 (0.26) and 0.10 (0.09); p=0.01), left (NPSLE/HCs: mean (SD)=0.16 (0.09) and 0.09 (0.05); p=0.01) and right superior parietal lobule (SPL) (NPSLE/HCs: mean (SD)=0.25 (0.19) and 0.13 (0.13), p=0.01) was noted in NPSLE versus HC groups. Among patients with NPSLE, verbal episodic memory scores were positively associated with connectivity (local efficiency) of the left hippocampus (r2=0.22, p=0.005) and negatively with local efficiency of the left angular gyrus (r2=0.24, p=0.003). Patients without NPSLE displayed hypoconnectivity of the right hippocampus (mean (SD)=0.056 (0.014)) and hyperconnectivity of the left angular gyrus (mean (SD)=0.25 (0.13)) and SPL (mean (SD)=0.17 (0.12)).ConclusionBy using dynamic CRQA of the rs-fMRI data, distorted FC was found globally, as well as in medial temporal and parietal brain regions in patients with SLE, that correlated significantly and adversely with memory capacity in NPSLE. These results highlight the value of dynamic approaches to assessing impaired brain network function in patients with lupus with and without neuropsychiatric symptoms.

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“…To date, this technique has been applied not only to neurological conditions characterized by severe perfusion disturbances, such as stroke [ 36 – 40 ], but also in patients with Alzheimer’s dementia or mild cognitive impairment [ 41 ], systemic lupus erythematosus [ 42 , 43 ], clinically isolated syndrome and multiple sclerosis [ 44 ], displaying more subtle hemodynamic impairment. By utilizing TSA on rs-fMRI data, it becomes possible to combine hemodynamic and functional connectivity metrics and assess the degree of their coupling (or uncoupling) within specific regions of the brain with the same technique and without the use of contrast agents.…”

Section: Introductionmentioning

confidence: 99%

Functional connectivity-hemodynamic (un)coupling changes in chronic mild brain injury are associated with mental health and neurocognitive indices: a resting state fMRI study

Kagialis,

Simos,

Manolitsi

et al. 2024

Neuroradiology

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Purpose To examine hemodynamic and functional connectivity alterations and their association with neurocognitive and mental health indices in patients with chronic mild traumatic brain injury (mTBI). Methods Resting-state functional MRI (rs-fMRI) and neuropsychological assessment of 37 patients with chronic mTBI were performed. Intrinsic connectivity contrast (ICC) and time-shift analysis (TSA) of the rs-fMRI data allowed the assessment of regional hemodynamic and functional connectivity disturbances and their coupling (or uncoupling). Thirty-nine healthy age- and gender-matched participants were also examined. Results Patients with chronic mTBI displayed hypoconnectivity in bilateral hippocampi and parahippocampal gyri and increased connectivity in parietal areas (right angular gyrus and left superior parietal lobule (SPL)). Slower perfusion (hemodynamic lag) in the left anterior hippocampus was associated with higher self-reported symptoms of depression (r = − 0.53, p = .0006) and anxiety (r = − 0.484, p = .002), while faster perfusion (hemodynamic lead) in the left SPL was associated with lower semantic fluency (r = − 0.474, p = .002). Finally, functional coupling (high connectivity and hemodynamic lead) in the right anterior cingulate cortex (ACC)) was associated with lower performance on attention and visuomotor coordination (r = − 0.50, p = .001), while dysfunctional coupling (low connectivity and hemodynamic lag) in the left ventral posterior cingulate cortex (PCC) and right SPL was associated with lower scores on immediate passage memory (r = − 0.52, p = .001; r = − 0.53, p = .0006, respectively). Uncoupling in the right extrastriate visual cortex and posterior middle temporal gyrus was negatively associated with cognitive flexibility (r = − 0.50, p = .001). Conclusion Hemodynamic and functional connectivity differences, indicating neurovascular (un)coupling, may be linked to mental health and neurocognitive indices in patients with chronic mTBI.

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Converging evidence of impaired brain function in systemic lupus erythematosus: changes in perfusion dynamics and intrinsic functional connectivity

Cited by 7 publications

References 39 publications

Resting‐State fMRI: Emerging Concepts for Future Clinical Application

Resting‐State fMRI: Emerging Concepts for Future Clinical Application

Altered hippocampal connectivity dynamics predicts memory performance in neuropsychiatric lupus: a resting-state fMRI study using cross-recurrence quantification analysis

Functional connectivity-hemodynamic (un)coupling changes in chronic mild brain injury are associated with mental health and neurocognitive indices: a resting state fMRI study

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