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Theta-burst transcranial magnetic stimulation induced functional connectivity changes between dorsolateral prefrontal cortex and default-mode-network

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Abstract

Functional connectivity (FC) is fundamental to brain function and has been implicated in many neuropsychological and neuropsychiatric disorders. It is then of great scientific and clinical interest to find a non-invasive approach to modulate FC. Transcranial magnetic stimulation (TMS) is a non-invasive neuromodulational tool that can affect the target region and remote brain areas. While the distributed effects of TMS are postulated to be through either structural or functional connectivity, an understudied but of great scientific interest question is whether TMS can change the FC between these regions. The purpose of this study was to address this question in normal healthy brain using TMS with continuous theta burst stimulation (cTBS) pulses, which are known to have long-lasting inhibition function. FC was calculated from resting state fMRI before and after real and control (SHAM) stimulation. Compared to SHAM, the repetitive TMS (rTMS) reduces FC between the cTBS target: the left dorsolateral prefrontal cortex (lDLPFC) and brain regions within the default mode network (DMN), proving the effects of rTMS on FC. The reduction of FC might be the results of the inhibitory effects of cTBS rTMS.

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References

  • Barker, A. T., Jalinous, R., & Freeston, I. L. (1985). Non-invasive magnetic stimulation of human motor cortex. The Lancet, 325(8437), 1106–1107.

    Google Scholar 

  • Biswal, B. B., Van Kylen, J., & Hyde, J. S. (1997). Simultaneous assessment of flow and BOLD signals in resting-state functional connectivity maps. NMR in Biomedicine, 10(4–5), 165–170.

    CAS  PubMed  Google Scholar 

  • Biswal, B., Yetkin, F. Z., Haughton, V. M., & Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic Resonance in Medicine, 34(4), 537–541.

    CAS  PubMed  Google Scholar 

  • Bolognini, N., & Ro, T. (2010). Transcranial magnetic stimulation: Disrupting neural activity to Alter and Assess brain function. Journal of Neuroscience, 30(29), 9647–9650.

    CAS  PubMed  Google Scholar 

  • Chan, R. W., Leong, A. T. L., Ho, L. C., Gao, P. P., Wong, E. C., Dong, C. M., et al. (2017). Low-frequency hippocampal-cortical activity drives brain-wide resting-state functional MRI connectivity. Proceedings of the National Academy of Sciences, 201703309.

  • Chen, A. C., Oathes, D. J., Chang, C., Bradley, T., Zhou, Z.-W., Williams, L. M., Glover, G. H., Deisseroth, K., & Etkin, A. (2013). Causal interactions between fronto-parietal central executive and default-mode networks in humans. Proceedings of the National Academy of Sciences, 110(49), 19944–19949.

    CAS  Google Scholar 

  • Cordes, D., Haughton, V., Carew, J. D., Arfanakis, K., & Maravilla, K. (2002). Hierarchical clustering to measure connectivity in fMRI resting-state data. Magnetic Resonance Imaging, 20(4), 305–317.

    PubMed  Google Scholar 

  • Cordes, D., Haughton, V. M., Arfanakis, K., Wendt, G. J., Turski, P. A., Moritz, C. H., et al. (2000). Mapping functionally related regions of brain with functional connectivity MR imaging. American Journal of Neuroradiology, 21(9), 1636–1644.

    CAS  PubMed  Google Scholar 

  • Curtis, C. E., & D’Esposito, M. (2003). Persistent activity in the prefrontal cortex during working memory. Trends in Cognitive Sciences, 7(9), 415–423.

    PubMed  Google Scholar 

  • Damoiseaux, J. S., Rombouts, S. A. R. B., Barkhof, F., Scheltens, P., Stam, C. J., Smith, S. M., & Beckmann, C. F. (2006). Consistent resting-state networks across healthy subjects. Proceedings of the National Academy of Sciences, 103(37), 13848–13853.

    CAS  Google Scholar 

  • De Luca, M., Smith, S., De Stefano, N., Federico, A., & Matthews, P. M. (2005). Blood oxygenation level dependent contrast resting state networks are relevant to functional activity in the neocortical sensorimotor system. Experimental Brain Research, 167(4), 587–594.

    PubMed  Google Scholar 

  • Donghui Song, D. C., Zhang, J., Ge, Q., Zang, Y.-F., & Ze, W. (2018). Associations of brain entropy (BEN) to cerebral blood flow and fractional amplitude of low-frequency fluctuations in the resting brain. Brain imaging and behavior.

  • Eldaief, M. C., Halko, M. A., Buckner, R. L., & Pascual-Leone, A. (2011). Transcranial magnetic stimulation modulates the brain’s intrinsic activity in a frequency-dependent manner. Proceedings of the National Academy of Sciences, 108(52), 21229–21234.

    CAS  Google Scholar 

  • Fan, J., McCandliss, B. D., Fossella, J., Flombaum, J. I., & Posner, M. I. (2005). The activation of attentional networks. NeuroImage, 26(2), 471–479.

    PubMed  Google Scholar 

  • Feredoes, E., Heinen, K., Weiskopf, N., Ruff, C., & Driver, J. (2011). Causal evidence for frontal involvement in memory target maintenance by posterior brain areas during distracter interference of visual working memory. Proceedings of the National Academy of Sciences, 108(42), 17510–17515.

    CAS  Google Scholar 

  • Fitzgerald. (2011). The effects of repetitive transcranial magnetic stimulation in the treatment of depression. Expert Review of Medical Devices, 8(1), 85–95.

    CAS  PubMed  Google Scholar 

  • Fitzgerald, P. B., Fountain, S., & Daskalakis, Z. J. (2006). A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clinical Neurophysiology, 117(12), 2584–2596.

    PubMed  Google Scholar 

  • Fox, M. D., Buckner, R. L., White, M. P., Greicius, M. D., & Pascual-Leone, A. (2012a). Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate. Biological Psychiatry, 72(7), 595–603.

    PubMed  PubMed Central  Google Scholar 

  • Fox, M. D., & Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews Neuroscience, 8(9), 700–711.

    CAS  PubMed  Google Scholar 

  • Fox, M., Halko, M., Eldaief, M., & Pascual-Leone, A. (2012b). Measuring and manipulating brain connectivity with resting state functional connectivity magnetic resonance imaging (fcMRI) and transcranial magnetic stimulation. Neuroimage, 62(4), 2232–2243.

    PubMed  PubMed Central  Google Scholar 

  • Fregni, F., & Pascual-Leone, A. (2007). Technology insight: Noninvasive brain stimulation in neurology - perspectives on the therapeutic potential of rTMS and tDCS. Nature Clinical Practice Neurology, 3(7), 383–393.

    PubMed  Google Scholar 

  • Friston, K. J. (1994). Functional and effective connectivity in neuroimaging:A synthesis. Human Brain Mapping, 2(2), 56–78.

    Google Scholar 

  • Friston, K. J., Williams, S., Howard, R., & Frackowiak, R. S. J. (1996). Movement-Related Effects in fMRI Time-Series.

  • Gratton, T. G. L. (2013). E. M. N. and M. D. Modelling Complex Networks: Cameo Graphs And Transport Processes, 7(Dec), 1–14.

    Google Scholar 

  • Gratton, C., Lee, T. G., Nomura, E. M., & D’Esposito, M. (2014). Perfusion MRI indexes variability in the functional brain effects of theta-burst transcranial magnetic stimulation. PLoS One, 9(7).

  • Greicius, M. D. (2008). Resting-state functional connectivity in neuropsychiatric disorders. Current Opinion in Neurology, 21(4), 424–430.

    PubMed  Google Scholar 

  • Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003). Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences, 100(1), 253–258.

    CAS  Google Scholar 

  • Heekeren, H. R., Marrett, S., Ruff, D. A., Bandettini, P. A., & Ungerleider, L. G. (2006). Involvement of human left dorsolateral prefrontal cortex in perceptual decision making is independent of response modality. Proceedings of the National Academy of Sciences, 103(26), 10023–10028.

    CAS  Google Scholar 

  • Huang, Y. Z., Edwards, M. J., Rounis, E., Bhatia, K. P., & Rothwell, J. C. (2005). Theta burst stimulation of the human motor cortex. Neuron, 45(2), 201–206.

    CAS  PubMed  Google Scholar 

  • Kobayashi, M., & Pascual-Leone, A. (2003). Transcranial magnetic stimulation in neurology. The Lancet Neurology, 2(3), 145–156.

    PubMed  Google Scholar 

  • Lowe, M. J., Dzemidzic, M., Lurito, J. T., Mathews, V. P., & Phillips, M. D. (2000). Correlations in low-frequency BOLD fluctuations reflect cortico-cortical connections. NeuroImage, 12(5), 582–587.

    CAS  PubMed  Google Scholar 

  • Lowe, M. J., Mock, B. J., & Sorenson, J. A. (1998). Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. NeuroImage, 7(2), 119–132.

    CAS  PubMed  Google Scholar 

  • Maeda, F., Keenan, J. P., Tormos, J. M., Topka, H., & Pascual-Leone, A. (2000). Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clinical Neurophysiology, 111, 800–805.

    CAS  PubMed  Google Scholar 

  • Mylius, V., Ayache, S. S., Ahdab, R., Farhat, W. H., Zouari, H. G., Belke, M., Brugières, P., Wehrmann, E., Krakow, K., Timmesfeld, N., Schmidt, S., Oertel, W. H., Knake, S., & Lefaucheur, J. P. (2013). Definition of DLPFC and M1 according to anatomical landmarks for navigated brain stimulation: Inter-rater reliability, accuracy, and influence of gender and age. NeuroImage, 78, 224–232.

    CAS  PubMed  Google Scholar 

  • Oberman, L., Edwards, D., Eldaief, M., & Pascual-Leone, A. (2011). Safety of theta burst transcranial magnetic stimulation: A systematic review of the literature. Journal of Clinical Neurophysiology, 28(1), 67–74.

    PubMed  PubMed Central  Google Scholar 

  • Orosz, A., Jann, K., Wirth, M., Wiest, R., Dierks, T., & Federspiel, A. (2012). Theta burst TMS increases cerebral blood flow in the primary motor cortex during motor performance as assessed by arterial spin labeling (ASL). NeuroImage, 61(3), 599–605.

    PubMed  Google Scholar 

  • Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences, 98(2), 676–682.

    CAS  Google Scholar 

  • Rossi, S., Hallett, M., Rossini, P. M., Pascual-Leone, A., Avanzini, G., Bestmann, S., et al. (2009). Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology, 120(12), 2008–2039.

    PubMed  PubMed Central  Google Scholar 

  • Rossini, P. M., & Rossi, S. (2007). Transcranial magnetic stimulation: Diagnostic, therapeutic, and research potential. Neurology, 68(7), 484–488.

    PubMed  Google Scholar 

  • Ruff, C. C., Driver, J., & Bestmann, S. (2009). Combining TMS and fMRI: From “virtual lesions” to functional-network accounts of cognition. Cortex, 45(9), 1043–1049.

    PubMed  Google Scholar 

  • Shang, Y.-Q., Xie, J., Peng, W., Zhang, J., Chang, D., & Wang, Z. (2018). Network-wise cerebral blood flow redistribution after 20 Hz rTMS on left dorso-lateral prefrontal cortex. European Journal of Radiology, 101, 144–148.

    PubMed  Google Scholar 

  • Siebner, H. R., Bergmann, T. O., Bestmann, S., Massimini, M., Johansen-Berg, H., Mochizuki, H., Bohning, D. E., Boorman, E. D., Groppa, S., Miniussi, C., Pascual-Leone, A., Huber, R., Taylor, P. C. J., Ilmoniemi, R. J., de Gennaro, L., Strafella, A. P., Kähkönen, S., Klöppel, S., Frisoni, G. B., George, M. S., Hallett, M., Brandt, S. A., Rushworth, M. F., Ziemann, U., Rothwell, J. C., Ward, N., Cohen, L. G., Baudewig, J., Paus, T., Ugawa, Y., & Rossini, P. M. (2009). Consensus paper: Combining transcranial stimulation with neuroimaging. Brain Stimulation, 2(2), 58–80.

    PubMed  Google Scholar 

  • Smittenaar, P., FitzGerald, T. H. B., Romei, V., Wright, N. D., & Dolan, R. J. (2013). Disruption of dorsolateral prefrontal cortex decreases model-based in favor of model-free control in humans. Neuron, 80(4), 914–919.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song, D., Chang, D., Zhang, J., Peng, W., Shang, Y., Gao, X., & Wang, Z. (2018). Reduced brain entropy by repetitive transcranial magnetic stimulation on the left dorsolateral prefrontal cortex in healthy young adults. Brain Imaging and Behavior.

  • Valero-Cabré, A., Payne, B. R., & Pascual-Leone, A. (2007). Opposite impact on 14C-2-deoxyglucose brain metabolism following patterns of high and low frequency repetitive transcranial magnetic stimulation in the posterior parietal cortex. Experimental Brain Research, 176(4), 603–615.

    PubMed  Google Scholar 

  • Valero-Cabré, A., Payne, B. R., Rushmore, J., Lomber, S. G., & Pascual-Leone, A. (2005). Impact of repetitive transcranial magnetic stimulation of the parietal cortex on metabolic brain activity: A 14C-2DG tracing study in the cat. Experimental Brain Research, 163(1), 1–12.

    PubMed  Google Scholar 

  • van den Heuvel, M., Mandl, R., & Pol, H. H. (2008). Normalized cut group clustering of resting-state fMRI data. PLoS One, 3(4).

  • Verdon, C.M., Saba, G. & Januel, D., (2004). Stimulation magnétique transcrânienne et fonctions cognitives. L'Encéphale, 30(4), 363–368.

  • Wagner, T., Valero-Cabre, A., & Pascual-Leone, A. (2007). Noninvasive human brain stimulation. Annual Review of Biomedical Engineering, 9(1), 527–565.

    CAS  PubMed  Google Scholar 

  • Wang, J. X., Rogers, L. M., Gross, E. Z., Ryals, A. J., Dokucu, M. E., Brandstatt, K. L., . . . Voss, J. L. (2014b). Targeted enhancement of cortical-hippocampal brain networks and associative memory Jane X. Wang, 1054.

  • Wang, Z., Aguirre, G. K., Rao, H., Wang, J., Fernández-Seara, M. A., Childress, A. R., & Detre, J. A. (2008). Empirical optimization of ASL data analysis using an ASL data processing toolbox: ASLtbx. Magnetic Resonance Imaging, 26(2), 261–269.

    PubMed  Google Scholar 

  • Wang, Z., Li, Y., Childress, A. R., & Detre, J. A. (2014a). Brain entropy mapping using fMRI. PLoS One, 9(3), 1–8.

    Google Scholar 

  • Wassermann, E. M., & Lisanby, S. H. (2001). Therapeutic application of repetitive transcranial magnetic stimulation: A review. Clinical Neurophysiology : Official Journal of the International Federation of Clinical Neurophysiology, 112, 1367–1377.

    CAS  Google Scholar 

  • Xiong, J. H., Parsons, L. M., Gao, J. H., & Fox, P. T. (1999). Interregional connectivity to primary motor cortex revealed using MRI resting state images. Human Brain Mapping, 8(2–3), 151–156.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xue, S. W., Guo, Y., Peng, W., Zhang, J., Chang, D., Zang, Y. F., & Wang, Z. (2017). Increased low-frequency resting-state brain activity by high-frequency repetitive TMS on the left dorsolateral prefrontal cortex. Frontiers in Psychology, 8(Dec), 1–8.

    Google Scholar 

  • Yan, C.-G., & Zang, Y.-F. (2010). DPARSF: A MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Frontiers in System Neuroscience, 4(May), 1–7.

    Google Scholar 

  • Zhang, D., & Raichle, M. E. (2010). Disease and the brain’s dark energy. Nature Reviews Neurology, 6(1), 15–28.

    PubMed  Google Scholar 

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Acknowledgements

This study was supported by National Natural Science Foundation of China (No. 61671198), the Youth 1000 Talent Program of China.

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Authors and Affiliations

  1. Center for Cognition and Brain Disorders, Institutes of Psychological Science, Hangzhou Normal University, Hangzhou, China

    Yuanqi Shang, Da Chang, Jian Zhang, Wei Peng, Donghui Song & Xin Gao

  2. Department of Diagnostic Radiology and Nuclear Medicine, University of Maryland School of Medicine, 670 W St, Room 1173, Baltimore, MD, 21201, USA

    Ze Wang

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  1. Yuanqi Shang
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Correspondence to Ze Wang.

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Shang, Y., Chang, D., Zhang, J. et al. Theta-burst transcranial magnetic stimulation induced functional connectivity changes between dorsolateral prefrontal cortex and default-mode-network. Brain Imaging and Behavior 14, 1955–1963 (2020). https://doi.org/10.1007/s11682-019-00139-y

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