Abstract
Premenstrual syndrome (PMS) is a menstrual cycle-related disorder. Previous studies have indicated alterations of brain functional connectivity in PMS patients. However, little is known about the overall organization of brain network in PMS patients. Functional magnetic resonance imaging data deriving from 20 PMS patients and 21 healthy controls (HCs). Pearson correlation between mean time-series was used to estimate connectivity matrix between each paired regions of interest, and the connectivity matrix for each participant was then binarized. Graph theory analysis was applied to assess each participant’s global and local topological properties of brain functional network. Correlation analysis was performed to evaluate relationships between the daily rating of severity of problems (DRSP) and abnormal network properties. PMS patients had lower small-worldness values than HCs. PMS-related alterations of nodal properties were mainly found in the posterior cingulate cortex, precuneus and angular gyrus. The PMS-related abnormal connectivity components were mainly associated with the thalamus, putamen and middle cingulate cortex. In the PMS group, the DRSP score were negatively correlated with the area under the curves of nodal local efficiency in the posterior cingulate cortex. Our study suggests that the graph-theory method may be one potential tool to detect disruptions of brain connections and may provide important evidence for understanding the PMS from the disrupted network organization perspective.
Similar content being viewed by others
Abbreviations
- PMS:
-
Premenstrual syndrome
- HCs:
-
Healthy controls
- HAMA:
-
Hamilton anxiety scale
- HAMD:
-
Hamilton depression scale
- DRSP:
-
Daily record of severity of problems
- BMI:
-
Body mass index
- Cp :
-
Clustering coefficients
- Lp :
-
Characteristic path lengths
- γ:
-
Normalized clustering coefficients
- λ:
-
Normalized characteristic path lengths
- σ:
-
Small-worldness
- Eg :
-
Network global efficiency
- Eloc :
-
Network local efficiency
- DC:
-
Degree centrality
- Ei :
-
Nodal efficiency
- NLe :
-
Nodal local efficiency
- NLp :
-
Node characteristic path length
- NCp :
-
Node clustering coefficient; The symbol “a” stands for the areas under the curves (AUC) of the topological metrics (Cp, Lp, γ, λ, σ, Eg, Eloc, DC, Ei, NLe, NLp, NCp)
- R:
-
Right
- L:
-
Left
- preCC:
-
Precentral cortex
- dlSFC:
-
Dorsolateral superior frontal cortex
- OFC:
-
Orbitofrontal cortex
- SMA:
-
Supplementary motor area
- SFC:
-
Superior frontal cortex
- MCC:
-
Middle cingulate cortex
- PCC:
-
Posterior cingulate cortex
- ANG:
-
Angular gyrus
- preCUN:
-
Precuneus
- PUT:
-
Putamen
- PAL:
-
Pallidum
- THA:
-
Thalamus
- STC:
-
Superior temporal cortex
- MTC:
-
Middle temporal cortex
Reference
Association, A. P. (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th ed. Washington, DC: American Psychiatric Press (3), 275–277.
Bao, A. M., Ji, Y. F., Van Someren, E. J., Hofman, M. A., Liu, R. Y., & Zhou, J. N. (2004). Diurnal rhythms of free estradiol and cortisol during the normal menstrual cycle in women with major depression. Hormones and Behavior, 45(2), 93–102.
Benito-Leon, J., Sanz-Morales, E., Melero, H., Louis, E. D., Romero, J. P., Rocon, E., et al. (2019). Graph theory analysis of resting-state functional magnetic resonance imaging in essential tremor. Human Brain Mapping, 40(16), 4686–4702.
Bu, L., Lai, Y., Deng, Y., Xiong, C., Li, F., Li, L., et al. (2019). Negative Mood Is Associated with Diet and Dietary Antioxidants in University Students During the Menstrual Cycle: A Cross-Sectional Study from Guangzhou, China. Antioxidants (basel), 9(1), 23.
Bullmore, E., & Sporns, O. (2009). Complex brain networks: Graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10(3), 186–198.
Calhoun, V. D., Wager, T. D., Krishnan, A., Rosch, K. S., Seymour, K. E., Nebel, M. B., et al. (2017). The impact of T1 versus EPI spatial normalization templates for fMRI data analyses. Human Brain Mapping, 38(11), 5331–5342.
Case, M., Shirinpour, S., Vijayakumar, V., Zhang, H., Datta, Y., Nelson, S., et al. (2019). Graph theory analysis reveals how sickle cell disease impacts neural networks of patients with more severe disease. Neuroimage Clinical, 21, 101599.
Cavanna, A. E., & Trimble, M. R. (2006). The precuneus: A review of its functional anatomy and behavioural correlates. Brain, 129(Pt 3), 564–583.
Chen, H., Sheng, X., Luo, C., Qin, R., Ye, Q., Zhao, H., et al. (2020). The compensatory phenomenon of the functional connectome related to pathological biomarkers in individuals with subjective cognitive decline. Translational Neurodegeneration, 9(1), 21.
De Bondt, T., Smeets, D., Pullens, P., Van Hecke, W., Jacquemyn, Y., & Parizel, P. M. (2015). Stability of resting state networks in the female brain during hormonal changes and their relation to premenstrual symptoms. Brain Research, 1624, 275–285.
Deng, D., Pang, Y., Duan, G., Liu, H., Liao, H., Liu, P., et al. (2018). Larger volume and different functional connectivity of the amygdala in women with premenstrual syndrome. European Radiology, 28(5), 1900–1908.
Duan, G., Liu, H., Pang, Y., Liu, P., Liu, Y., Wang, G., et al. (2018). Hippocampal fractional amplitude of low-frequency fluctuation and functional connectivity changes in premenstrual syndrome. Journal of Magnetic Resonance Imaging, 47(2), 545–553.
Elsenbruch, S., Rosenberger, C., Enck, P., Forsting, M., Schedlowski, M., & Gizewski, E. R. (2010). Affective disturbances modulate the neural processing of visceral pain stimuli in irritable bowel syndrome: An fMRI study. Gut, 59(4), 489–495.
Filippi, M., van den Heuvel, M. P., Fornito, A., He, Y., Hulshoff Pol, H. E., Agosta, F., et al. (2013). Assessment of system dysfunction in the brain through MRI-based connectomics. Lancet Neurology, 12(12), 1189–1199.
Halbreich, U., Backstrom, T., Eriksson, E., O’Brien, S., Calil, H., Ceskova, E., et al. (2007). Clinical diagnostic criteria for premenstrual syndrome and guidelines for their quantification for research studies. Gynecological Endocrinology, 23(3), 123–130.
Jin, M., Wang, L., Wang, H., Han, X., Diao, Z., Guo, W., et al. (2020). Altered resting-state functional networks in patients with hemodialysis: a graph-theoretical based study. Brain Imaging and Behavior, 15(2), 833–845.
Le, J., Thomas, N., & Gurvich, C. (2020). Cognition, The Menstrual Cycle, and Premenstrual Disorders: A Review. Brain Sciences, 10(4), 198.
Lee, L. C., Chen, Y. H., Lin, C. S., Li, W. C., Low, I., Tu, C. H., et al. (2018). Unaltered intrinsic functional brain architecture in young women with primary dysmenorrhea. Science and Reports, 8(1), 12971.
Liang, X., Wang, J., Yan, C., Shu, N., Xu, K., Gong, G., et al. (2012). Effects of different correlation metrics and preprocessing factors on small-world brain functional networks: a resting-state functional MRI study. PLoS ONE, 7(3), e32766.
Liao, H., Duan, G., Liu, P., Liu, Y., Pang, Y., Liu, H., et al. (2017a). Altered fractional amplitude of low frequency fluctuation in premenstrual syndrome: A resting state fMRI study. Journal of Affective Disorders, 218, 41–48.
Liao, H., Pang, Y., Liu, P., Liu, H., Duan, G., Liu, Y., et al. (2017b). Abnormal Spontaneous Brain Activity in Women with Premenstrual Syndrome Revealed by Regional Homogeneity. Frontiers in Human Neuroscience, 11, 62.
Liu, F., Wang, Y., Li, M., Wang, W., Li, R., Zhang, Z., et al. (2017a). Dynamic functional network connectivity in idiopathic generalized epilepsy with generalized tonic-clonic seizure. Human Brain Mapping, 38(2), 957–973.
Liu, P., Li, R., Bao, C., Wei, Y., Fan, Y., Liu, Y., et al. (2018a). Altered topological patterns of brain functional networks in Crohn’s disease. Brain Imaging and Behavior, 12(5), 1466–1478.
Liu, P., Wei, Y., Fan, Y., Li, R., Liu, Y., Wang, G., et al. (2018b). Altered brain structure in women with premenstrual syndrome. Journal of Affective Disorders, 229, 239–246.
Liu, P., Wei, Y., Liao, H., Fan, Y., Li, R., Feng, N., et al. (2018c). Thalamocortical dysconnectivity in premenstrual syndrome. Brain Imaging and Behavior, 13(3), 717–724.
Liu, P., Zeng, F., Zhou, G., Wang, J., Wen, H., von Deneen, K. M., et al. (2013). Alterations of the default mode network in functional dyspepsia patients: A resting-state fmri study. Neurogastroenterology and Motility, 25(6), 382–388.
Liu, Q., Li, R., Zhou, R., Li, J., & Gu, Q. (2015). Abnormal Resting-State Connectivity at Functional MRI in Women with Premenstrual Syndrome. PLoS ONE, 10(9), e0136029.
Liu, Q., Wang, Y., van Heck, C. H., & Qiao, W. (2017b). Stress reactivity and emotion in premenstrual syndrome. Neuropsychiatric Disease and Treatment, 13, 1597–1602.
Liu, Y., Liang, M., Zhou, Y., He, Y., Hao, Y., Song, M., et al. (2008). Disrupted small-world networks in schizophrenia. Brain, 131(4), 945–961.
Pereira, J. B., Mijalkov, M., Kakaei, E., Mecocci, P., Vellas, B., Tsolaki, M., et al. (2016). Disrupted Network Topology in Patients with Stable and Progressive Mild Cognitive Impairment and Alzheimer’s Disease. Cerebral Cortex, 26(8), 3476–3493.
Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage, 59(3), 2142–2154.
Power, J. D., Schlaggar, B. L., Lessov-Schlaggar, C. N., & Petersen, S. E. (2013). Evidence for hubs in human functional brain networks. Neuron, 79(4), 798–813.
Quintana-Zinn, F. A., Whitcomb, B. W., Ronnenberg, A. G., Bigelow, C., Houghton, S. C., & Bertone-Johnson, E. R. (2017). Premenstrual Symptom Patterns and Behavioral Risk Factors in Young Women: A Cross-Sectional Study. Journal of Women’s Health (2002), 26(10), 1099–1105.
Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: Uses and interpretations. NeuroImage, 52(3), 1059–1069.
Ryu, A., & Kim, T. H. (2015). Premenstrual syndrome: A mini review. Maturitas, 82(4), 436–440.
Song, K., Li, J., Zhu, Y., Ren, F., Cao, L., Shao, Y., et al. (2021). Altered small-world functional network topology in patients with optic neuritis: A resting-state fMRI study. Dis Markers, 2021, 9948751.
Sreenivasan, K., Mishra, V., Bird, C., Zhuang, X., Yang, Z., Cordes, D., et al. (2019). Altered functional network topology correlates with clinical measures in very early-stage, drug-naive Parkinson’s disease. Parkinsonism & Related Disorders, 62, 3–9.
Sun, Y., Collinson, S. L., Suckling, J., & Sim, K. (2018). Dynamic Reorganization of Functional Connectivity Reveals Abnormal Temporal Efficiency in Schizophrenia. Schizophrenia Bulletin, 45(3), 659–669.
Tolossa, F. W., & Bekele, M. L. (2014). Prevalence, impacts and medical managements of premenstrual syndrome among female students cross-sectional study in college of health sciences. BMC Women’s Health, 14, 52.
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273–289.
van den Heuvel, M. P., & Hulshoff Pol, H. E. (2010). Exploring the brain network: A review on resting-state fMRI functional connectivity. European Neuropsychopharmacology, 20(8), 519–534.
Wang, J., Wang, L., Zang, Y., Yang, H., Tang, H., Gong, Q., et al. (2009). Parcellation-dependent small-world brain functional networks: A resting-state fMRI study. Human Brain Mapping, 30(5), 1511–1523.
Wang, J., Wang, X., He, Y., Yu, X., Wang, H., & He, Y. (2015a). Apolipoprotein E ε4 modulates functional brain connectome in Alzheimer’s disease. Human Brain Mapping, 36(5), 1828–1846.
Wang, J., Wang, X., Xia, M., Liao, X., Evans, A., & He, Y. (2015b). GRETNA: A graph theoretical network analysis toolbox for imaging connectomics. Frontiers in Human Neuroscience, 9, 386.
Wang, Y., Zheng, L., Liu, Y., Ye, Y., Luo, S., Lu, G., et al. (2019). The gut microbiota-inflammation-brain axis in end-stage renal disease: Perspectives from default mode network. Theranostics, 9(26), 8171–8181.
Wu, H., Sun, H., Wang, C., Yu, L., Li, Y., Peng, H., et al. (2016a). Abnormalities in the structural covariance of emotion regulation networks in major depressive disorder. Journal of Psychiatric Research, 84, 237–242.
Wu, M., Liang, Y., Wang, Q., Zhao, Y., & Zhou, R. (2016b). Emotion Dysregulation of Women with Premenstrual Syndrome. Science and Reports, 6(38501), 1–10.
Wu, Y., Wang, C., Qian, W., Yu, L., Xing, X., Wang, L., et al. (2020). Disrupted default mode network dynamics in recuperative patients of herpes zoster pain. CNS Neuroscience & Therapeutics, 00, 1–10.
Yang, X., Liu, J., Meng, Y., Xia, M., Cui, Z., Wu, X., et al. (2017). Network analysis reveals disrupted functional brain circuitry in drug-naive social anxiety disorder. NeuroImage, 190, 213–223.
Van der Werf, Y. D., Witter, M. P., & Groenewegen, H. J. (2002). The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Research Reviews, 39(2–3), 107–140.
Zhang, J., Wang, J., Wu, Q., Kuang, W., Huang, X., He, Y., et al. (2011). Disrupted brain connectivity networks in drug-naive, first-episode major depressive disorder. Biological Psychiatry, 70(4), 334–342.
Funding
This study was financially supported by the National Natural Science Foundation of China under Grant Nos. 81771918, 82060315 and 81760886; Shaanxi Natural Science Foundation under Grant No. 2020JM-197; Guangxi Natural Science Foundation under Grant No. 2016GXNSFAA380086; and Fundamental Research Funds for the Central Universities under Grant No. XJS201202.
This study was authorized by the Medicine Ethics Committee of First Affiliated Hospital, Guangxi University of Chinese Medicine. All the research processes for this study were performed in consistent with the Declaration of Helsinki.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Liu, C., Xuan, C., Wu, J. et al. Altered resting-state functional networks in patients with premenstrual syndrome: a graph-theoretical based study. Brain Imaging and Behavior 16, 435–444 (2022). https://doi.org/10.1007/s11682-021-00518-4
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-021-00518-4