Thalamocortical dysconnectivity in premenstrual syndrome

  • Peng Liu
  • Ying Wei
  • Hai Liao
  • Yingying Fan
  • Ru Li
  • Nana Feng
  • Gaoxiong Duan
  • Demao Deng
  • Wei Qin
Original Research


Premenstrual syndrome (PMS) is a menstrual cycle-related disorder. Although the precise pathophysiology is not fully understood, it is increasingly believed that the central nervous system plays a vital role in the development of PMS. The aim of this study is to elucidate specific functional connectivity between the thalamus and cerebral cortex. Resting-state functional magnetic resonance imaging (fMRI) data were obtained from 20 PMS patients and 21 healthy controls (HCs). Seed-based functional connectivity between the thalamus and six cortical regions of interest, including the prefrontal cortex (PFC), posterior parietal cortex, somatosensory cortex, motor cortex/supplementary motor area, temporal and occipital lobe, was adopted to identify specific thalamocortical connectivity in the two groups. Correlation analysis was then used to examine relationships between the neuroimaging findings and clinical symptoms. Activity in distinct cortical regions correlated with specific sub-regions of the thalamus in the two groups. Comparison between groups exhibited decreased prefrontal-thalamic connectivity and increased posterior parietal–thalamic connectivity in the PMS patients. Within the PMS group, the daily record of severity of problems (DRSP) score negatively correlated with the prefrontal-thalamic connectivity. Our findings may provide preliminary evidence for abnormal thalamocortical connectivity in PMS patients and may contribute to a better understanding of the pathophysiology of PMS.


Premenstrual syndrome Functional magnetic resonance imaging Functional connectivity Thalamus 



This work was supported by the National Natural Science Foundation of China under Grant Nos. 81771918, 81471738, 81471811 and 81760886; National Basic Research Program of China under Grant Nos. 2014CB543203 and 2015CB856403; Guangxi Natural Science Foundation under Grant Nos. 2016GXNSFAA380006 and 2017GXNSFBA198095; Natural Science Basic Research Plan in Shaanxi Province of China under Grant No. 2017JM6051; and the Fundamental Research Funds for the Central Universities.

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial interests.

Ethical approval

The experiment procedures were approved by the Medicine Ethics Committee of First Affiliated Hospital, Guangxi University of Chinese Medicine, Guangxi, China. Each research procedure of this study was conducted in accordance with the Declaration of Helsinki. All participants provided written informed consent after receiving an explanation of the whole study.


  1. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders, fifth edition (DSM-5). Washington, DC: American Psychiatric Press.CrossRefGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. Bishop, S., Duncan, J., Brett, M., & Lawrence, A. D. (2004). Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli. Nature Neuroscience, 7(2), 184–188.CrossRefPubMedGoogle Scholar
  4. Bondt, T. D., Smeets, D., Pullens, P., Hecke, W. V., 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.CrossRefPubMedGoogle Scholar
  5. Byne, W., Buchsbaum, M. S., Mattiace, L. A., Hazlett, E. A., Kemether, E., Elhakem, S. L., Purohit, D. P., Haroutunian, V., & Jones, L. (2002). Postmortem assessment of thalamic nuclear volumes in subjects with schizophrenia. American Journal of Psychiatry, 159(1), 59–65.CrossRefPubMedGoogle Scholar
  6. Calhoun, V. D., Wager, T. D., Krishnan, A., Rosch, K. S., Seymour, K. E., Nebel, M. B., Mostofsky, S. H., Nyalakanai, P., & Kiehl, K. (2017). The impact of T1 versus EPI spatial normalization templates for fMRI data analyses. Human Brain Mapping, 38(11), 5331–5342.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chao-Gan, Y., & Yu-Feng, Z. (2010). DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Frontiers in Systems Neuroscience, 4, 13. Scholar
  8. Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3(3), 201–215.CrossRefPubMedGoogle Scholar
  9. Davidson, R. J. (2002). Anxiety and affective style: role of prefrontal cortex and amygdala. Biological Psychiatry, 51(1), 68–80.CrossRefPubMedGoogle Scholar
  10. Dixon, M. L., Thiruchselvam, R., Todd, R., & Christoff, K. (2017). Emotion and the prefrontal cortex: an integrative review. Psychological Bulletin, 143(10), 1033–1081.CrossRefPubMedGoogle Scholar
  11. Duan, G., Liu, H., Pang, Y., Liu, P., Liu, Y., Wang, G., Liao, H., Tang, L., Chen, W., Mo, X., Wen, D., Lin, H., & Deng, D. (2018). Hippocampal fractional amplitude of low-frequency fluctuation and functional connectivity changes in premenstrual syndrome. Journal of Magnetic Resonance Imaging, 47(2), 545–553.CrossRefPubMedGoogle Scholar
  12. Endicott, J., Nee, J., & Harrison, W. (2006). Daily record of severity of problems (DRSP): reliability and validity. Archives of Women’s Mental Health, 9(1), 41–49.CrossRefPubMedGoogle Scholar
  13. Fadgyasstanculete, M., Buga, A. M., Popawagner, A., & Dumitrascu, D. L. (2014). The relationship between irritable bowel syndrome and psychiatric disorders: from molecular changes to clinical manifestations. Journal of Molecular Psychiatry, 2(1), 4.CrossRefGoogle Scholar
  14. Failla, M. D., Peters, B. R., Karbasforoushan, H., Foss-Feig, J. H., Schauder, K. B., Heflin, B. H., & Cascio, C. J. (2017). Intrainsular connectivity and somatosensory responsiveness in young children with ASD. Molecular Autism, 8(1), 25.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Frye, M. A., Watzl, J., Banakar, S., O'Neill, J., Mintz, J., Davanzo, P., Fischer, J., Chirichigno, J. W., Ventura, J., Elman, S., Tsuang, J., Walot, I., & Thomas, M. A. (2007). Increased anterior cingulate/medial prefrontal cortical glutamate and creatine in bipolar depression. Neuropsychopharmacology, 32(12), 2490–2499.CrossRefPubMedGoogle Scholar
  16. Goldin, P. R., Manber, T., Hakimi, S., Canli, T., & Gross, J. J. (2009). Neural bases of social anxiety disorder: emotional reactivity and cognitive regulation during social and physical threat. Archives of General Psychiatry, 66(2), 170–180. Scholar
  17. Greene, C. M., Flannery, O., & Soto, D. (2014). Distinct parietal sites mediate the influences of mood, arousal, and their interaction on human recognition memory. Cognitive, Affective, & Behavioral Neuroscience, 14(4), 1327–1339.CrossRefGoogle Scholar
  18. Greicius, M. D., Flores, B. H., Menon, V., Glover, G. H., Solvason, H. B., Kenna, H., Reiss, A. L., & Schatzberg, A. F. (2007). Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biological Psychiatry, 62(5), 429–437.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Haber, S. N. (2003). The primate basal ganglia: parallel and integrative networks. Journal of Chemical Neuroanatomy, 26(4), 317–330.CrossRefPubMedGoogle Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. Jr, M. D. (2005). Premenstrual disorders: epidemiology and disease burden. The American Journal of Managed Care, 11(16 Suppl), 473–479.Google Scholar
  22. Kim, U., Sanchez-Vives, M. V., & Mccormick, D. A. (1997). Functional dynamics of GABAergic inhibition in the thalamus. Science, 278(5335), 130–134.CrossRefPubMedGoogle Scholar
  23. Liao, H., Duan, G., Liu, P., Liu, Y., Pang, Y., Liu, H., Tang, L., Tao, J., Wen, D., Li, S., Liang, L., & Deng, D. (2017a). Altered fractional amplitude of low frequency fluctuation in premenstrual syndrome: a resting state fMRI study. Journal of Affective Disorders, 218, 41–48.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Liu, P., Wei, Y., Fan, Y., Li, R., Liu, Y., Wang, G., Wei, Y., Pang, Y., Deng, D., & Qin, W. (2018). Altered brain structure in women with premenstrual syndrome. Journal of Affective Disorders, 229, 239–246. Scholar
  27. Nair, A., Treiber, J. M., Shukla, D. K., Shih, P., & Müller, R. A. (2013). Impaired thalamocortical connectivity in autism spectrum disorder: a study of functional and anatomical connectivity. Brain, 136(6), 1942–1955.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Nevatte, T., O’Brien, P. M. S., Bäckström, T., Brown, C., Dennerstein, L., Endicott, J., et al. (2013). ISPMD consensus on the management of premenstrual disorders. Archives of Women’s Mental Health, 16(4), 279–291.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ridderinkhof, K. R., Ullsperger, M., Crone, E. A., & Nieuwenhuis, S. (2004). The role of the medial frontal cortex in cognitive control. Science, 306(5695), 443–447.CrossRefPubMedGoogle Scholar
  30. Ryu, A., & Kim, T. H. (2015). Premenstrual syndrome: a mini review. Maturitas, 82(4), 436–440. Scholar
  31. Saalmann, Y. B. (2014). Intralaminar and medial thalamic influence on cortical synchrony, information transmission and cognition. Frontiers in Systems Neuroscience, 8(83), 83.PubMedPubMedCentralGoogle Scholar
  32. Seminowicz, D. A., Labus, J. S., Bueller, J. A., Tillisch, K., Naliboff, B. D., Bushnell, M. C., et al. (2010). Regional gray matter density changes in brains of patients with irritable bowel syndrome. Gastroenterology, 139(1), 48–57 e42. Scholar
  33. Sestieri, C., Shulman, G. L., & Corbetta, M. (2010). Attention to memory and the environment: functional specialization and dynamic competition in human posterior parietal cortex. Journal of Neuroscience, 30(25), 8445–8456.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Sestieri, C., Shulman, G. L., & Corbetta, M. (2017). The contribution of the human posterior parietal cortex to episodic memory. Nature Reviews. Neuroscience, 18(3), 183–192. Scholar
  35. Sherman, S. M. (2001). Exploring the thalamus. Elsevier. Google Scholar
  36. Skåtun, K. C., Kaufmann, T., Brandt, C. L., Doan, N. T., Alnæs, D., Tønnesen, S., et al. (2017). Thalamo-cortical functional connectivity in schizophrenia and bipolar disorder. Brain Imaging and Behavior, 1–13.Google Scholar
  37. Smith, M. J., Adams, L. F., Schmidt, P. J., Rubinow, D. R., & Wassermann, E. M. (2003). Abnormal luteal phase excitability of the motor cortex in women with premenstrual syndrome. Biological Psychiatry, 54(7), 757–762.CrossRefPubMedGoogle Scholar
  38. Tadayonnejad, R., Ajilore, O., Mickey, B. J., Crane, N. A., Hsu, D. T., Kumar, A., Zubieta, J. K., & Langenecker, S. A. (2016). Pharmacological modulation of pulvinar resting-state regional oscillations and network dynamics in major depression. Psychiatry Research, 252, 10–18.CrossRefPubMedCentralPubMedGoogle Scholar
  39. Wang, D., Zhang, X., Zhang, X., Huang, Z., & Song, Y. (2017). Magnetic resonance imaging analysis of brain function in patients with irritable bowel syndrome. BMC Gastroenterology, 17(1), 148. Scholar
  40. Woodward, N. D., Karbasforoushan, H., & Heckers, S. (2012). Thalamocortical dysconnectivity in schizophrenia. American Journal of Psychiatry, 169(10), 1092–1099.CrossRefPubMedGoogle Scholar
  41. Yan, C. G., Wang, X. D., Zuo, X. N., & Zang, Y. F. (2016). DPABI: data processing & analysis for (resting-state) brain imaging. Neuroinformatics, 14(3), 339–351. Scholar
  42. Zarei, M., Patenaude, B., Damoiseaux, J., Morgese, C., Smith, S., Matthews, P. M., Barkhof, F., Rombouts, S., Sanz-Arigita, E., & Jenkinson, M. (2010). Combining shape and connectivity analysis: an MRI study of thalamic degeneration in Alzheimer's disease. NeuroImage, 49(1), 1–8.CrossRefPubMedGoogle Scholar
  43. Zhang, D., Snyder, A. Z., Fox, M. D., Sansbury, M. W., Shimony, J. S., & Raichle, M. E. (2008). Intrinsic functional relations between human cerebral cortex and thalamus. Journal of Neurophysiology, 100(4), 1740–1748.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Zhang, D., Snyder, A. Z., Shimony, J. S., Fox, M. D., & Raichle, M. E. (2010). Noninvasive functional and structural connectivity mapping of the human thalamocortical system. Cerebral Cortex, 20(5), 1187–1194.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Life Sciences Research Center, School of Life Science and TechnologyXidian UniversityXi’anChina
  2. 2.Engineering Research Center of Molecular and Neuro Imaging, Ministry of Education, School of Life Science and TechnologyXidian UniversityXi’anChina
  3. 3.Department of RadiologyFirst Affiliated Hospital of Guangxi University of Chinese MedicineNanningChina

Personalised recommendations