Skip to main content

The Location Reliability of the Resting-State fMRI FC of Emotional Regions Towards rTMS Therapy

Abstract

Resting-state magnetic resonance imaging (RS-fMRI) studies indicated that the repetitive transcranial magnetic stimulation (rTMS) exerts antidepression effect through the functional connectivity (FC) of the DLPFC with the subgenual anterior cingulate cortex (sgACC), pregneual ACC (pgACC), or nucleus accumbens (NAc). It is proposed that the FC-guided individualized precise stimulation on the DLPFC would be more effective. The current study systematically investigated the reliability of the RS-fMRI FC location as well as the FC strength with multiple potential factors. We aimed to provide a stable stimulation target for future FC-guided TMS therapy for affective related disorders. Twenty-one subjects under RS-fMRI conditions with the first two times (V1, V2) scanned on a GE 3 T scanner and the third visit (V3) on a Siemens 3 T scanner. Then the FC strength and location reliability were assessed by using intra-class correlation (ICC) and intra-individual distance, respectively. The factors included deep seed ROIs (midline (mid-) sgACC, left pgACC, mid-pgACC, and left NAc), eyes closed (EC) vs eyes open (EO), frequency bands, FC algorithm (Pearson vs Spearman), scanning length (half a session vs whole session), and location method (FC peak vs center of gravity (COG)). The reliability of the voxel-wise FC strength was low to moderate. The intra-individual distances of the COG were 3.8–7.3 mm across all factors, much smaller than that of FC peak (approximately 30 mm). The COG of seed-based FC might be a potential rTMS stimulation target. Anyway, all potential stimulation targets should be tested in future rTMS treatment studies.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Admon, R., Kaiser, R. H., Dillon, D. G., Beltzer, M., Goer, F., Olson, D. P., Vitaliano, G., & Pizzagalli, D. A. (2017, Apr 1). Dopaminergic Enhancement of Striatal Response to Reward in Major Depression. American Journal of Psychiatry, 174(4), 378–386. https://doi.org/10.1176/appi.ajp.2016.16010111

  • Baldessarini, R. J., Lau, W. K., Sim, J., Sum, M. Y., & Sim, K. (2015, Feb). Duration of initial antidepressant treatment and subsequent relapse of major depression. Journal Clinical Psychopharmacology, 35(1), 75–76. https://doi.org/10.1097/jcp.0000000000000263

  • Berlim, M. T., van den Eynde, F., Tovar-Perdomo, S., & Daskalakis, Z. J. (2014, Jan). Response, remission and drop-out rates following high-frequency repetitive transcranial magnetic stimulation (rTMS) for treating major depression: a systematic review and meta-analysis of randomized, double-blind and sham-controlled trials. Psychological Medicine, 44(2), 225–239. https://doi.org/10.1017/s0033291713000512

  • Cao, X., Deng, C., Su, X., & Guo, Y. (2018). Response and Remission Rates Following High-Frequency vs. Low-Frequency Repetitive Transcranial Magnetic Stimulation (rTMS) Over Right DLPFC for Treating Major Depressive Disorder (MDD): A Meta-Analysis of Randomized, Double-Blind Trials. Frontiers in Psychiatry, 9, 413. https://doi.org/10.3389/fpsyt.2018.00413

  • Cash, R. F. H., Cocchi, L., Lv, J., Fitzgerald, P. B., & Zalesky, A. (2021a, Mar 1). Functional magnetic resonance imaging-guided personalization of transcranial magnetic stimulation treatment for depression. JAMA Psychiatry, 78(3), 337–339. https://doi.org/10.1001/jamapsychiatry.2020.3794

  • Cash, R. F. H., Cocchi, L., Lv, J., Wu, Y., Fitzgerald, P. B., & Zalesky, A. (2021b, Feb 5). Personalized connectivity-guided DLPFC-TMS for depression: Advancing computational feasibility, precision and reproducibility. Human Brain Mapping. https://doi.org/10.1002/hbm.25330

  • Cash, R. F. H., Zalesky, A., Thomson, R. H., Tian, Y., Cocchi, L., & Fitzgerald, P. B. (2019, Jul 15). Subgenual functional connectivity predicts antidepressant treatment response to transcranial magnetic stimulation: Independent validation and evaluation of personalization. Biological Psychiatry, 86(2), e5-e7. https://doi.org/10.1016/j.biopsych.2018.12.002

  • Chen, J., Zhou, C., Wu, B., Wang, Y., Li, Q., Wei, Y., Yang, D., Mu, J., Zhu, D., Zou, D., & Xie, P. (2013, Dec 30). Left versus right repetitive transcranial magnetic stimulation in treating major depression: a meta-analysis of randomised controlled trials. Psychiatry Research, 210(3), 1260–1264. https://doi.org/10.1016/j.psychres.2013.09.007

  • Ciric, R., Wolf, D. H., Power, J. D., Roalf, D. R., Baum, G. L., Ruparel, K., Shinohara, R. T., Elliott, M. A., Eickhoff, S. B., Davatzikos, C., Gur, R. C., Gur, R. E., Bassett, D. S., & Satterthwaite, T. D. (2017, Jul 1). Benchmarking of participant-level confound regression strategies for the control of motion artifact in studies of functional connectivity. Neuroimage, 154, 174–187. https://doi.org/10.1016/j.neuroimage.2017.03.020

  • Deng, Z. D., Lisanby, S. H., & Peterchev, A. V. (2014, Jun). Coil design considerations for deep transcranial magnetic stimulation. Clinical Neurophysiology, 125(6), 1202–1212. https://doi.org/10.1016/j.clinph.2013.11.038

  • Du, L., Liu, H., Du, W., Chao, F., Zhang, L., Wang, K., Huang, C., Gao, Y., & Tang, Y. (2018, Mar 9). Stimulated left DLPFC-nucleus accumbens functional connectivity predicts the anti-depression and anti-anxiety effects of rTMS for depression. Translational Psychiatry, 7(11), 3. https://doi.org/10.1038/s41398-017-0005-6

  • Ernst, J., Hock, A., Henning, A., Seifritz, E., Boeker, H., & Grimm, S. (2017, Jan). Increased pregenual anterior cingulate glucose and lactate concentrations in major depressive disorder. Molecular Psychiatry, 22(1), 113–119. https://doi.org/10.1038/mp.2016.73

  • Fox, M. D., Buckner, R. L., White, M. P., Greicius, M. D., & Pascual-Leone, A. (2012, Oct 1). Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate. Biological Psychiatry, 72(7), 595–603. https://doi.org/10.1016/j.biopsych.2012.04.028

  • Jing, Y., Zhao, N., Deng, X. P., Feng, Z. J., Huang, G. F., Meng, M., Zang, Y. F., & Wang, J. (2020, Apr). Pregenual or subgenual anterior cingulate cortex as potential effective region for brain stimulation of depression. Brain and Behavior, 10(4), e01591. https://doi.org/10.1002/brb3.1591

  • Langenecker, S. A., Kennedy, S. E., Guidotti, L. M., Briceno, E. M., Own, L. S., Hooven, T., Young, E. A., Akil, H., Noll, D. C., & Zubieta, J. K. (2007, Dec 1). Frontal and limbic activation during inhibitory control predicts treatment response in major depressive disorder. Biological Psychiatry, 62(11), 1272–1280. https://doi.org/10.1016/j.biopsych.2007.02.019

  • Long, Z., Du, L., Zhao, J., Wu, S., Zheng, Q., & Lei, X. (2020). Nov 1). Prediction on treatment improvement in depression with resting state connectivity: A coordinate-based meta-analysis. Journal of Affective Disorders, 276, 62–68. https://doi.org/10.1016/j.jad.2020.06.072

    Article  PubMed  Google Scholar 

  • Ma, Y. (2015, Mar). Neuropsychological mechanism underlying antidepressant effect: a systematic meta-analysis. Molecular Psychiatry, 20(3), 311–319. https://doi.org/10.1038/mp.2014.24

  • Malhi, G. S., & Mann, J. J. (2018, Nov 24). Depression. Lancet, 392(10161), 2299-2312. https://doi.org/10.1016/s0140-6736(18)31948-2

  • Ning, L., Makris, N., Camprodon, J. A., & Rathi, Y. (2019, Jan-Feb). Limits and reproducibility of resting-state functional MRI definition of DLPFC targets for neuromodulation. Brain Stimulation, 12(1), 129–138. https://doi.org/10.1016/j.brs.2018.10.004

  • Noble, S., Scheinost, D., & Constable, R. T. (2019, Dec). A decade of test-retest reliability of functional connectivity: A systematic review and meta-analysis. Neuroimage, 203, 116157. https://doi.org/10.1016/j.neuroimage.2019.116157

  • Noble, S., Scheinost, D., Finn, E. S., Shen, X., Papademetris, X., McEwen, S. C., Bearden, C. E., Addington, J., Goodyear, B., Cadenhead, K. S., Mirzakhanian, H., Cornblatt, B. A., Olvet, D. M., Mathalon, D. H., McGlashan, T. H., Perkins, D. O., Belger, A., Seidman, L. J., Thermenos, H., … & Constable, R. T. (2017, Feb 1). Multisite reliability of MR-based functional connectivity. NeuroImage, 146, 959–970. https://doi.org/10.1016/j.neuroimage.2016.10.020

  • Noble, S., Spann, M. N., Tokoglu, F., Shen, X., Constable, R. T., & Scheinost, D. (2017b, Nov 1). Influences on the Test-Retest Reliability of Functional Connectivity MRI and its Relationship with Behavioral Utility. Cereb Cortex, 27(11), 5415–5429. https://doi.org/10.1093/cercor/bhx230

  • Otte, C., Gold, S. M., Penninx, B. W., Pariante, C. M., Etkin, A., Fava, M., Mohr, D. C., & Schatzberg, A. F. (2016, Sep 15). Major depressive disorder. Nature Reviews Disease Primers , 2, 16065. https://doi.org/10.1038/nrdp.2016.65

  • Pizzagalli, D., Pascual-Marqui, R. D., Nitschke, J. B., Oakes, T. R., Larson, C. L., Abercrombie, H. C., Schaefer, S. M., Koger, J. V., Benca, R. M., & Davidson, R. J. (2001, Mar). Anterior cingulate activity as a predictor of degree of treatment response in major depression: evidence from brain electrical tomography analysis. American Journal of Psychiatry, 158(3), 405–415. https://doi.org/10.1176/appi.ajp.158.3.405

  • Pizzagalli, D. A. (2011, Jan). Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacology, 36(1), 183–206. https://doi.org/10.1038/npp.2010.166

  • Ren, X., Yu, S., Dong, W., Yin, P., Xu, X., & Zhou, M. (2020, May 1). Burden of depression in China, 1990–2017: Findings from the global burden of disease study 2017. Journal of Affective Disorders, 268, 95–101. https://doi.org/10.1016/j.jad.2020.03.011

  • Rossini, P. M., Burke, D., Chen, R., Cohen, L. G., Daskalakis, Z., Di Iorio, R., Di Lazzaro, V., Ferreri, F., Fitzgerald, P. B., George, M. S., Hallett, M., Lefaucheur, J. P., Langguth, B., Matsumoto, H., Miniussi, C., Nitsche, M. A., Pascual-Leone, A., Paulus, W., Rossi, S., Rothwell, J. C., Siebner, H. R., Ugawa, Y., Walsh, V., & Ziemann, U. (2015, Jun). Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: Basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clinical Neurophysiology, 126(6), 1071–1107. https://doi.org/10.1016/j.clinph.2015.02.001

  • Rush, A. J., Trivedi, M. H., Wisniewski, S. R., Nierenberg, A. A., Stewart, J. W., Warden, D., Niederehe, G., Thase, M. E., Lavori, P. W., Lebowitz, B. D., McGrath, P. J., Rosenbaum, J. F., Sackeim, H. A., Kupfer, D. J., Luther, J., & Fava, M. (2006, Nov). Acute and longer-term outcomes in depressed outpatients requiring one or several treatment steps: a STAR*D report. American Journal of Psychiatry, 163(11), 1905–1917. https://doi.org/10.1176/ajp.2006.163.11.1905

  • Shrout, P. E., & Fleiss, J. L. (1979, Mar). Intraclass correlations: uses in assessing rater reliability. Psychol Bull, 86(2), 420–428. https://doi.org/10.1037/00332909.86.2.420

  • Somandepalli, K., Kelly, C., Reiss, P. T., Zuo, X. N., Craddock, R. C., Yan, C. G., Petkova, E., Castellanos, F. X., Milham, M. P., & Di Martino, A. (2015, Oct). Short-term test-retest reliability of resting state fMRI metrics in children with and without attention-deficit/hyperactivity disorder. Developmental Cognitive Neuroscience, 15, 83–93. https://doi.org/10.1016/j.dcn.2015.08.003

  • Wassermann, E. M., & Zimmermann, T. (2012, Jan). Transcranial magnetic brain stimulation: therapeutic promises and scientific gaps. Pharmacology & Therapeutics, 133(1), 98–107. https://doi.org/10.1016/j.pharmthera.2011.09.003

  • Weigand, A., Horn, A., Caballero, R., Cooke, D., Stern, A. P., Taylor, S. F., Press, D., Pascual-Leone, A., & Fox, M. D. (2018, Jul 1). Prospective validation that subgenual connectivity predicts antidepressant efficacy of transcranial magnetic stimulation sites. Biological Psychiatry, 84(1), 28–37. https://doi.org/10.1016/j.biopsych.2017.10.028

  • Yan, C. G., Wang, X. D., Zuo, X. N., & Zang, Y. F. (2016, Jul). DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging. Neuroinformatics, 14(3), 339–351. https://doi.org/10.1007/s12021-016-9299-4

  • Yuan, L. X., Wang, J. B., Zhao, N., Li, Y. Y., Ma, Y., Liu, D. Q., He, H. J., Zhong, J. H., & Zang, Y. F. (2018). Intra- and Inter-scanner Reliability of Scaled Subprofile Model of Principal Component Analysis on ALFF in Resting-State fMRI Under Eyes Open and Closed Conditions. Frontiers in Neuroscience, 12, 311. https://doi.org/10.3389/fnins.2018.00311

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao, N., Yuan, L. X., Jia, X. Z., Zhou, X. F., Deng, X. P., He, H. J., Zhong, J., Wang, J., & Zang, Y. F. (2018). Intra- and Inter-Scanner Reliability of Voxel-Wise Whole-Brain Analytic Metrics for Resting State fMRI. Frontiers in Neuroinformatics, 12, 54. https://doi.org/10.3389/fninf.2018.00054

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou, M., Hu, X., Lu, L., Zhang, L., Chen, L., Gong, Q., & Huang, X. (2017, Apr 3). Intrinsic cerebral activity at resting state in adults with major depressive disorder: A meta-analysis. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 75, 157–164. https://doi.org/10.1016/j.pnpbp.2017.02.001

  • Zuo, X. N., & Xing, X. X. (2014, Sep). Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: A systems neuroscience perspective. Neuroscience and Biobehavioral Reviews, 45, 100–118. https://doi.org/10.1016/j.neubiorev.2014.05.009

Download references

Funding

This work was supported by the Key Realm R&D Program of Guangdong Province (2019B030335001), the National Natural Science Foundation of China (NSFC) (82071537, 81520108016), Key Medical Discipline of Hangzhou, and The Cultivation Project of the Province-leveled Preponderant Characteristic Discipline of Hangzhou Normal University (18JYXK046, 20JYXK004).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yu-Tao Xiang or Yu-Feng Zang.

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.

Supplementary file1 (DOCX 6837 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhao, N., Yue, J., Feng, ZJ. et al. The Location Reliability of the Resting-State fMRI FC of Emotional Regions Towards rTMS Therapy. Neuroinform (2022). https://doi.org/10.1007/s12021-022-09585-4

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12021-022-09585-4

Keywords

  • Functional connectivity
  • Reliability
  • rTMS
  • Major depression disorder