To explore the relationship between brain function changes and clinical serological indicators and behavioral cognitive assessment in patients with neuropsychiatric systemic lupus erythematosus (NPSLE), and understand the pathogenesis of NPSLE from the perspective of imaging.
Methods
The resting-state functional imaging data, clinical serological, and behavioral cognitive assessment scores of 28 patients with NPSLE and 22 healthy controls (HC) were prospectively collected. The resting-state amplitude of low-frequency fluctuation (ALFF) values obtained from the analysis and processing were correlated with the serological data and behavioral cognitive assessment scores to determine the relationship between these data.
Results
The average age of the patients of the NPSLE group was older than that of the HC group; significant differences in education level, Auditory Verbal Learning Test Hua Shan Version (AVLT-H), and Trail Making Test scores were observed between the two groups. The NPSLE group demonstrated increased brain activity in the insula, precentral gyrus, and superior temporal gyrus, and decreased brain activity in the superior parietal gyrus. The ALFF value of the insula positively correlated with the Anti-β2gp1 antibody and negatively correlated with the anti-nucleosome antibody and the AVL-recall (RC) score. The ALFF of the precentral gyrus negatively correlated with the AVL-immediate recall (I). The ALFF value of the superior temporal gyrus negatively correlated with the AVL-RC score. The left superior parietal gyrus positively correlated with the c-reactive protein. The right superior parietal gyrus positively correlated with the System Lupus Erythematosus Disease Activity Index and negatively correlated with the AVL-I score.
Conclusion
Patients with NPSLE show different brain activity changes in different brain regions, and the abnormal brain regions are correlated with certain lupus antibodies, inflammatory factors, and cognitive assessment, thereby suggesting that the correlation between the three could provide novel insights into the pathogenesis of NPSLE.
The American college of rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum1999; 42: 599–608. DOI: 10.1002/1529-0131. (199904)42:4<599::AID-ANR2>3.0.CO;2-F.
2.
SchwartzNStockADPuttermanC. Neuropsychiatric lupus: new mechanistic insights and future treatment directions. Nat Rev Rheumatol2019; 15: 137–152. DOI: 10.1038/s41584-018-0156-8
3.
YuHQiuXZhangY-Q, et al.Abnormal amplitude of low frequency fluctuation and functional connectivity in non-neuropsychiatric systemic lupus erythematosus: a resting-state fMRI study. Neuroradiology2019; 61: 331–340. DOI: 10.1007/s00234-018-2138-6.
4.
LiuSChengYXieZ, et al.A conscious resting state fMRI study in SLE patients without major neuropsychiatric manifestations. Front Psychiatr2018; 9: 677. DOI: 10.3389/fpsyt.2018.00677
5.
BonacchiRRoccaMARamirezGA, et al.Resting state network functional connectivity abnormalities in systemic lupus erythematosus: correlations with neuropsychiatric impairment. Mol Psychiatr2021; 26: 3634–3645. DOI: 10.1038/s41380-020-00907-z
6.
BombardierCGladmanDDUrowitzMB, et al.Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum1992; 35: 630–640
7.
LiPDingDMaXY, et al.Altered intrinsic brain activity and memory performance improvement in patients with end-stage renal disease during a single dialysis session. Brain Imaging Behav2018; 12: 1640–1649. DOI: 10.1007/s11682-018-9828-x
8.
OlsonIRPlotzkerAEzzyatY. The Enigmatic temporal pole: a review of findings on social and emotional processing. Brain: A Journal of Neurology2007; 130: 1718–1731.
9.
GiordanoBLEspositoMValenteG, et al.Intermediate acoustic-to-semantic representations link behavioral and neural responses to natural sounds. Nat Neurosci2023; 26: 664–672. DOI: 10.1038/s41593-023-01285-9
10.
LongQLiWZhangW, et al.Electrical stimulation mapping in the medial prefrontal cortex induced auditory hallucinations of episodic memory: a case report. Front Hum Neurosci2022; 16: 815232. DOI: 10.3389/fnhum.2022.815232
11.
Ortega-de San LuisCRyanTJ. Understanding the physical basis of memory: molecular mechanisms of the engram. J Biol Chem2022; 298: 101866. DOI: 10.1016/j.jbc.2022.101866
12.
El-KallinyMMWittigJHSheehanTC, et al.Changing temporal context in human temporal lobe promotes memory of distinct episodes. Nat Commun2019; 10: 203. DOI: 10.1038/s41467-018-08189-4
13.
LjunggrenSAndersson-RoswallLImbergH, et al.Predicting verbal memory decline following temporal lobe resection for epilepsy. Acta Neurol Scand2019; 140: 312–319. DOI: 10.1111/ane.13146
14.
FleuryMBuckSBindingLP, et al.Episodic memory network connectivity in temporal lobe epilepsy. Epilepsia2022; 63: 2597–2622. DOI: 10.1111/epi.17370
15.
WangYJiangMHuangL, et al.Altered functional brain network in systemic lupus erythematosus patients without overt neuropsychiatric symptoms based on resting-state functional magnetic resonance imaging and multivariate pattern analysis. Front Neurol2021; 12: 690979. DOI: 10.3389/fneur.2021.690979
16.
WuB-BMaYXieL, et al.Impaired decision-making and functional neuronal network activity in systemic lupus erythematosus. J Magn Reson Imag: JMRI2018; 48: 1508–1517. DOI: 10.1002/jmri.26006
YapleZArsalidouM. N-Back working memory task: meta-analysis of normative fMRI studies with children. Child Dev2018; 89: 2010–2022. DOI: 10.1111/cdev.13080
19.
NayaYYoshidaMMiyashitaY. Forward processing of long-term associative memory in monkey inferotemporal cortex. J Neurosci: Official J Soc Neuro2003; 23: 2861–2871.
20.
BalderasIRodriguez-OrtizCJBermudez-RattoniF. Consolidation and reconsolidation of object recognition memory. Behav Brain Res2015; 285: 213–222. DOI: 10.1016/j.bbr.2014.08.049
21.
SuzukiWANayaY. The perirhinal cortex. Annu Rev Neurosci2014; 37: 39–53. DOI: 10.1146/annurev-neuro-071013-014207
22.
NayaYYoshidaMTakedaM, et al.Delay-period activities in two subdivisions of monkey inferotemporal cortex during pair association memory task. Eur J Neurosci2003; 18: 2915–2918.
23.
Ameen-AliKESivakumaranMHEacottMJ, et al.Perirhinal cortex and the recognition of relative familiarity. Neurobiol Learn Mem2021; 182: 107439. DOI: 10.1016/j.nlm.2021.107439
24.
MirandaMBekinschteinP. Plasticity mechanisms of memory consolidation and reconsolidation in the perirhinal cortex. Neuroscience2018; 370: 46–61. DOI: 10.1016/j.neuroscience.2017.06.002
25.
ZhouCDongMDuanW, et al.White matter microstructure alterations in systemic lupus erythematosus: a preliminary coordinate-based meta-analysis of diffusion tensor imaging studies. Lupus2021; 30: 1973–1982. DOI: 10.1177/09612033211045062
26.
JániMKašpárekT. Emotion recognition and theory of mind in schizophrenia: a meta-analysis of neuroimaging studies. World J Biol Psychiatr: The Offi J World Feder Soc Bio Psy2018; 19: S86–S96. DOI: 10.1080/15622975.2017.1324176
27.
GuoPHuSJiangX, et al.Associations of neurocognition and social cognition with brain structure and function in early-onset schizophrenia. Front Psychiatr2022; 13: 798105. DOI: 10.3389/fpsyt.2022.798105
28.
LaneH-YTuC-HLinW-C, et al.Brain activity of benzoate, a D-amino acid oxidase inhibitor, in patients with mild cognitive impairment in a randomized, double-blind, placebo controlled clinical trial. Int J Neuropsychopharmacol2021; 24: 392–399. DOI: 10.1093/ijnp/pyab001
29.
Teixeira-MachadoLAridaRMde Jesus MariJ. Dance for neuroplasticity: a descriptive systematic review. Neurosci Biobehav Rev2019; 96: 232–240. DOI: 10.1016/j.neubiorev.2018.12.010
30.
BizzoBCSanchezTATukamotoG, et al.Cortical thickness and episodic memory impairment in systemic lupus erythematosus. J Neuroimaging: Offi J of the American Soc Neuro2017; 27: 122–127. DOI: 10.1111/jon.12394
31.
ZhaoLTanXWangJ, et al.Brain white matter structural networks in patients with non-neuropsychiatric systemic lupus erythematosus. Brain Imaging and Behavior2018; 12: 142–155. DOI: 10.1007/s11682-017-9681-3
32.
HoRCThiaghuCOngH, et al.A meta-analysis of serum and cerebrospinal fluid autoantibodies in neuropsychiatric systemic lupus erythematosus. Autoimmun Rev2016; 15: 124–138. DOI: 10.1016/j.autrev.2015.10.003
Magro-ChecaCKumarSRamiroS, et al.Are serum autoantibodies associated with brain changes in systemic lupus erythematosus? MRI data from the Leiden NP-SLE cohort. Lupus2019; 28: 94–103. DOI: 10.1177/0961203318816819
35.
MokCCLauCSWongRW. Neuropsychiatric manifestations and their clinical associations in southern Chinese patients with systemic lupus erythematosus. J Rheumatol2001; 28: 766–771.
36.
MustonenPLehtonenKVJavelaK, et al.Persistent antiphospholipid antibody (aPL) in asymptomatic carriers as a risk factor for future thrombotic events: a nationwide prospective study. Lupus2014; 23: 1468–1476. DOI: 10.1177/0961203314545410
37.
DengXLiuX. Reevaluation of predictive value of ACL and anti-β2GP1 antibody for thrombosis in patients with systemic lupus erythematosus: from a perspective of a practical world. Rheumatol Int2012; 32: 3881–3886. DOI: 10.1007/s00296-011-2267-2
38.
XiaoYLinYZhangY, et al.Factors associated with the antinuclear antibody (ANA) titer of systemic autoimmune rheumatic diseases in ANA-positive patients after treatment: a retrospective study. Clin Exp Med2022; 22: 439–446. DOI: 10.1007/s10238-021-00759-z
39.
SuYJiaR-LHanL, et al.Role of anti-nucleosome antibody in the diagnosis of systemic lupus erythematosus. Clin Immunol2007; 122: 115–120.
40.
CappellettiMLeeHLFreemanED, et al.The role of right and left parietal lobes in the conceptual processing of numbers. J Cognit Neurosci2010; 22: 331–346. DOI: 10.1162/jocn.2009.21246
41.
O'DonovanABahorikASidneyS, et al.Relationships of inflammation trajectories with white matter volume and integrity in midlife. Brain Behav Immun2021; 91: 81–88. DOI: 10.1016/j.bbi.2020.09.006
42.
DevSIMooreRCSoontornniyomkijB, et al.Peripheral inflammation related to lower fMRI activation during a working memory task and resting functional connectivity among older adults: a preliminary study. Int J Geriatr Psychiatr2017; 32: 341–349. DOI: 10.1002/gps.4482
