Functional Dysconnectivity and Microstructural Impairment of the Cortico-thalamo-cortical Network in Women with Rheumatoid Arthritis: A Multimodal MRI Study

Overview

Journal Heliyon

Specialty Social Sciences

Date 2024 Feb 2

PMID 38304809

Authors

Yanmin Zheng

Lei Xie

Zikai Huang

Jianhua Peng

Shuxin Huang

Ruiwei Guo

Jinzhuang Huang

Zhirong Lin

Zelin Zhuang

Jingjing Yin

Zhiduo Hou

Shuhua Ma

Affiliations

Soon will be listed here.

Abstract

Background: Cognitive deficits are common in rheumatoid arthritis (RA) patients, but the mechanisms remain unclear. We investigated the effective connectivity and structural alterations of the core brain regions in RA patients with cognitive impairment.

Methods: Twenty-four female patients with RA and twenty-four healthy controls were enrolled. We analyzed abnormal brain activity patterns using functional MRI during the Iowa gambling task (IGT) and core regions effective connectivity using dynamic causal model (DCM). Structural alterations of white matter volume (WMV) and gray matter volume (GMV) were detected using voxel-based morphometry (VBM).

Results: RA patients showed altered activation patterns of the cortico-thalamo-cortical network, increased coupling strength from the left ventromedial prefrontal gyrus to the anterior cingulate cortex (ACC), the ACC to the right thalamus, and decreased connectivity from the thalamus to left hippocampus. VBM structural analysis showed increased GMV in the bilateral orbital frontal gyrus, bilateral hippocampus and right putamen, and reduced GMV and WMV in the bilateral thalamus in RA patients. Right thalamic GMV and WMV were positively correlated with the right thalamus-to-hippocampus connective strength. Additionally, the bold signal, GMV and WMV of the right thalamus were positively correlated with cognitive performance (IGT score) in RA patients.

Conclusion: Results suggest a structural and functional deficiency in the cortico-thalamo-cortical network, which is characterized by increased ACC-to-thalamus strength and reduced thalamus-to-hippocampus coupling in RA patients. The cognitive dysfunction may be the result of compensatory measures against imbalanced cortico-thalamic-cortical coupling.

References

Aggleton J, McMacKin D, Carpenter K, Hornak J, Kapur N, Halpin S . Differential cognitive effects of colloid cysts in the third ventricle that spare or compromise the fornix. Brain. 2000; 123 ( Pt 4):800-15. DOI: 10.1093/brain/123.4.800. View

Xiao D, Zikopoulos B, Barbas H . Laminar and modular organization of prefrontal projections to multiple thalamic nuclei. Neuroscience. 2009; 161(4):1067-81. PMC: 2700123. DOI: 10.1016/j.neuroscience.2009.04.034. View

Giguere M, Goldman-Rakic P . Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys. J Comp Neurol. 1988; 277(2):195-213. DOI: 10.1002/cne.902770204. View

Farrar D, Mian A, Budson A, Moss M, Killiany R . Functional brain networks involved in decision-making under certain and uncertain conditions. Neuroradiology. 2017; 60(1):61-69. PMC: 5798459. DOI: 10.1007/s00234-017-1949-1. View

Guillery R, Sherman S . Branched thalamic afferents: what are the messages that they relay to the cortex?. Brain Res Rev. 2010; 66(1-2):205-19. PMC: 3657838. DOI: 10.1016/j.brainresrev.2010.08.001. View

Bechara A, Damasio A, Damasio H, Anderson S . Insensitivity to future consequences following damage to human prefrontal cortex. Cognition. 1994; 50(1-3):7-15. DOI: 10.1016/0010-0277(94)90018-3. View

Goldman-Rakic P, Porrino L . The primate mediodorsal (MD) nucleus and its projection to the frontal lobe. J Comp Neurol. 1985; 242(4):535-60. DOI: 10.1002/cne.902420406. View

Tikasz A, Dumais A, Lipp O, Stip E, Lalonde P, Laurelli M . Reward-related decision-making in schizophrenia: A multimodal neuroimaging study. Psychiatry Res Neuroimaging. 2019; 286:45-52. DOI: 10.1016/j.pscychresns.2019.03.007. View

Aletaha D, Neogi T, Silman A, Funovits J, Felson D, Bingham 3rd C . 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Ann Rheum Dis. 2010; 69(9):1580-8. DOI: 10.1136/ard.2010.138461. View

10.

Schrepf A, Kaplan C, Ichesco E, Larkin T, Harte S, Harris R . A multi-modal MRI study of the central response to inflammation in rheumatoid arthritis. Nat Commun. 2018; 9(1):2243. PMC: 5993749. DOI: 10.1038/s41467-018-04648-0. View

11.

Isseroff A, ROSVOLD H, GALKIN T, Goldman-Rakic P . Spatial memory impairments following damage to the mediodorsal nucleus of the thalamus in rhesus monkeys. Brain Res. 1982; 232(1):97-113. DOI: 10.1016/0006-8993(82)90613-8. View

12.

ODoherty J, Hampton A, Kim H . Model-based fMRI and its application to reward learning and decision making. Ann N Y Acad Sci. 2007; 1104:35-53. DOI: 10.1196/annals.1390.022. View

13.

McDowell B, Marr C, Holmes C, Edwards C, Cardwell C, McHenry M . Prevalence of cognitive impairment in patients with rheumatoid arthritis: a cross sectional study. BMC Psychiatry. 2022; 22(1):777. PMC: 9733399. DOI: 10.1186/s12888-022-04417-w. View

14.

Jones E . Thalamic circuitry and thalamocortical synchrony. Philos Trans R Soc Lond B Biol Sci. 2003; 357(1428):1659-73. PMC: 1693077. DOI: 10.1098/rstb.2002.1168. View

15.

Vassilaki M, Crowson C, Davis III J, Duong S, Jones D, Nguyen A . Rheumatoid Arthritis, Cognitive Impairment, and Neuroimaging Biomarkers: Results from the Mayo Clinic Study of Aging. J Alzheimers Dis. 2022; 89(3):943-954. PMC: 9535562. DOI: 10.3233/JAD-220368. View

16.

Kaplan C, Schrepf A, Ichesco E, Larkin T, Harte S, Harris R . Association of Inflammation With Pronociceptive Brain Connections in Rheumatoid Arthritis Patients With Concomitant Fibromyalgia. Arthritis Rheumatol. 2019; 72(1):41-46. DOI: 10.1002/art.41069. View

17.

Pergola G, Danet L, Pitel A, Carlesimo G, Segobin S, Pariente J . The Regulatory Role of the Human Mediodorsal Thalamus. Trends Cogn Sci. 2018; 22(11):1011-1025. PMC: 6198112. DOI: 10.1016/j.tics.2018.08.006. View

18.

Roy D, Zhang Y, Halassa M, Feng G . Thalamic subnetworks as units of function. Nat Neurosci. 2022; 25(2):140-153. PMC: 9400132. DOI: 10.1038/s41593-021-00996-1. View

19.

Schlecht M, Jayachandran M, Rasch G, Allen T . Dual projecting cells linking thalamic and cortical communication routes between the medial prefrontal cortex and hippocampus. Neurobiol Learn Mem. 2022; 188:107586. PMC: 8851867. DOI: 10.1016/j.nlm.2022.107586. View

20.

Wallin K, Solomon A, Kareholt I, Tuomilehto J, Soininen H, Kivipelto M . Midlife rheumatoid arthritis increases the risk of cognitive impairment two decades later: a population-based study. J Alzheimers Dis. 2012; 31(3):669-76. DOI: 10.3233/JAD-2012-111736. View