Highlights
- •Several connectivity were decreased in cognitively impaired patients with NMOSD.
- •Decreased connectivity were associated with worse cognitive performance.
- •Intranetwork connectivity in the pDMN were decreased in cognitively impaired patients.
- •Internetwork connectivity between SN and pDMN/rFPN were decreased in cognitively impaired patients.
Abstract
Background
Cognitive impairment is one of the common symptoms in patients with neuromyelitis
optica spectrum disorder (NMOSD). However, the underlying mechanism remains unclear.
Resting-state functional magnetic resonance imaging (rs-fMRI) offers the opportunity
to reveal the patterns of brain activity in patients with different cognitive states.
Accordingly, this study investigated functional connectivity (FC) abnormalities within
and between the main cognitive networks in cognitively impaired (CI) patients with
NMOSD and their correlations with cognitive performance.
Methods
Thirty-four patients with NMOSD and 39 healthy controls (HC) were included. Neuropsychological
evaluations and rs-fMRI scanning were performed. Patients were classified as CI (n = 16) or cognitively preserved (CP; n = 18) according to neuropsychological evaluations. Seven components representing
six main cognitive networks were selected by group independent component analysis.
The differences in inter- and intranetwork FC among CI, CP, and HC groups were assessed.
The correlation between FC values and neuropsychological data in NMOSD was calculated.
Results
The CI group showed decreased intranetwork connectivity in the posterior default mode
network (pDMN) compared with the HC group (P < 0.05, GRF corrected), and decreased internetwork connectivity between the salience
network (SN) and pDMN, and between the SN and right frontoparietal network (rFPN)
compared with CP and HC groups. The altered FC values were significantly correlated
with cognitive performance in the whole NMOSD group.
Conclusion
The disconnection within the pDMN and between the SN and pDMN or rFPN might suggest
the neural substrates underlying cognitive impairment in NMOSD.
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Multiple Sclerosis and Related DisordersAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Tracking whole-brain connectivity dynamics in the resting state.Cereb. Cortex. 2014; 24: 663-676https://doi.org/10.1093/cercor/bhs352
- White matter atrophy and cognitive dysfunctions in neuromyelitis optica.PLoS One. 2012; 7: e33878https://doi.org/10.1371/journal.pone.0033878
- The brain's default network: anatomy, function, and relevance to disease.Ann. N. Y. Acad. Sci. 2008; 1124: 1-38https://doi.org/10.1196/annals.1440.011
- Large-scale functional network connectivity mediate the associations of gut microbiota with sleep quality and executive functions.Hum. Brain Mapp. 2021; 42: 3088-3101https://doi.org/10.1002/hbm.25419
- Spatial and temporal independent component analysis of functional MRI data containing a pair of task-related waveforms.Hum. Brain Mapp. 2001; 13: 43-53https://doi.org/10.1002/hbm.1024
- Early predictors of disability of paediatric-onset AQP4-IgG-seropositive neuromyelitis optica spectrum disorders.J. Neurol. Neurosurg. Psychiatry. 2022; 93: 101-111https://doi.org/10.1136/jnnp-2021-327206
- DPARSF: A MATLAB toolbox for "pipeline" data analysis of resting-state fMRI.Front. Syst. Neurosci. 2010; 4https://doi.org/10.3389/fnsys.2010.00013
- Brain structural and functional reorganization in tinnitus patients without hearing loss after sound therapy: a preliminary longitudinal study.Front. Neurosci. 2021; 15573858https://doi.org/10.3389/fnins.2021.573858
- Cognitive impairment in NMOSD-More questions than answers.Brain Behav. 2020; 10: e01842https://doi.org/10.1002/brb3.1842
- The human brain is intrinsically organized into dynamic, anticorrelated functional networks.Proc. Natl. Acad. Sci. U. S. A. 2005; 102: 9673-9678https://doi.org/10.1073/pnas.0504136102
- A rating scale for depression.J. Neurol. Neurosurg. Psychiatry. 1960; 23: 56-62https://doi.org/10.1136/jnnp.23.1.56
- Functional connectivity alterations in neuromyelitis optica spectrum disorder: correlation with disease duration and cognitive impairment.Clin. Neuroradiol. 2020; 30: 559-568https://doi.org/10.1007/s00062-019-00802-3
- Mechanisms of network changes in cognitive impairment in multiple sclerosis.Neurology. 2021; 97: e1886-e1897https://doi.org/10.1212/WNL.0000000000012834
- Multimodal magnetic resonance imaging in relation to cognitive impairment in neuromyelitis optica spectrum disorder.Sci. Rep. 2017; 7: 9180https://doi.org/10.1038/s41598-017-08889-9
- The role of the posterior cingulate cortex in cognition and disease.Brain. 2014; 137: 12-32https://doi.org/10.1093/brain/awt162
- Large-scale brain network coupling predicts acute nicotine abstinence effects on craving and cognitive function.JAMA Psychiatry. 2014; 71: 523-530https://doi.org/10.1001/jamapsychiatry.2013.4091
- Structural MRI substrates of cognitive impairment in neuromyelitis optica.Neurology. 2015; 85: 1491-1499https://doi.org/10.1212/wnl.0000000000002067
- Mayo's Older African Americans normative studies: norms for Boston Naming Test, controlled oral word association, category fluency, animal naming, token test, WRAT-3 reading, trail making test, stroop test, and judgment of line orientation.Clin. Neuropsychol. 2005; 19: 243-269https://doi.org/10.1080/13854040590945337
- Electrophysiological signatures of resting state networks in the human brain.Proc. Natl. Acad. Sci. U. S. A. 2007; 104: 13170-13175https://doi.org/10.1073/pnas.0700668104
- Large-scale brain networks and psychopathology: a unifying triple network model.Trends Cogn. Sci. 2011; 15: 483-506https://doi.org/10.1016/j.tics.2011.08.003
- The effects of methylphenidate on whole brain intrinsic functional connectivity.Hum. Brain Mapp. 2014; 35: 5379-5388https://doi.org/10.1002/hbm.22557
- Cognitive impairment in neuromyelitis optica spectrum disorders: a review of clinical and neuroradiological features.Front Neurol. 2019; 10: 608https://doi.org/10.3389/fneur.2019.00608
- Functional network organization of the human brain.Neuron. 2011; 72: 665-678https://doi.org/10.1016/j.neuron.2011.09.006
- The montreal cognitive assessment: creating a crosswalk with the mini-mental state examination.J. Am. Geriatr. Soc. 2015; 63: 2370-2374https://doi.org/10.1111/jgs.13710
- Cognitive impairment and cortical degeneration in neuromyelitis optica.Ann. Neurol. 2013; 73: 65-76https://doi.org/10.1002/ana.23721
- Functional brain connectivity abnormalities and cognitive deficits in neuromyelitis optica spectrum disorder.Mult. Scler. 2020; 26: 795-805https://doi.org/10.1177/1352458519845109
- Network attributes for segregation and integration in the human brain.Curr. Opin. Neurobiol. 2013; 23: 162-171https://doi.org/10.1016/j.conb.2012.11.015
- Mayo's Older Americans Normative studies: age- and IQ-adjusted norms for the trail-making test, the stroop test, and MAE controlled oral word association test.Clin. Neuropsychol. 2005; 19: 329-377https://doi.org/10.1080/13854040590945210
- Cognitive behavioral therapy may rehabilitate abnormally functional communication pattern among the triple-network in major depressive disorder: a follow-up study.J. Affect. Disord. 2022; 304: 28-39https://doi.org/10.1016/j.jad.2022.02.050
- Hamilton rating scale for anxiety (HAM-A).Occup. Med. 2015; 65 (Lond): 601https://doi.org/10.1093/occmed/kqv054
- International consensus diagnostic criteria for neuromyelitis optica spectrum disorders.Neurology. 2015; 85: 177-189https://doi.org/10.1212/WNL.0000000000001729
- Competition between frontoparietal control and default networks supports social working memory and empathy.Soc. Cogn. Affect. Neurosci. 2015; 10: 1144-1152https://doi.org/10.1093/scan/nsu160
- DPABI: data processing & analysis for (resting-state) brain imaging.Neuroinformatics. 2016; 14: 339-351https://doi.org/10.1007/s12021-016-9299-4
- Cognitive characteristics in Chinese non-demented PD patients based on gender difference.Transl. Neurodegener. 2018; 7https://doi.org/10.1186/s40035-018-0120-1
- Reduced GABA levels in the medial prefrontal cortex are associated with cognitive impairment in patients with NMOSD.Mult. Scler. Relat. Disord. 2022; 58103496https://doi.org/10.1016/j.msard.2022.103496
- Cognitive impairment in Chinese neuromyelitis optica.Mult. Scler. 2015; 21: 1839-1846https://doi.org/10.1177/1352458515576982
- The shape trail test: application of a new variant of the trail making test.PLoS One. 2013; 8: e57333https://doi.org/10.1371/journal.pone.0057333
- Altered structural networks in neuromyelitis optica spectrum disorder related with cognition impairment and clinical features.Mult. Scler. Relat. Disord. 2021; 48102714https://doi.org/10.1016/j.msard.2020.102714
- Predicting regional neurodegeneration from the healthy brain functional connectome.Neuron. 2012; 73: 1216-1227https://doi.org/10.1016/j.neuron.2012.03.004
Article info
Publication history
Published online: August 13, 2022
Accepted:
August 13,
2022
Received in revised form:
August 7,
2022
Received:
February 17,
2022
Identification
Copyright
© 2022 Elsevier B.V. All rights reserved.