Volume 41 Issue 4
Jul.  2020
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Qing-Bo Lu, Jian-Fei Sun, Qu-Yang Yang, Wen-Wen Cai, Meng-Qin Xia, Fang-Fang Wu, Ning Gu, Zhi-Jun Zhang. Magnetic brain stimulation using iron oxide nanoparticle-mediated selective treatment of the left prelimbic cortex as a novel strategy to rapidly improve depressive-like symptoms in mice. Zoological Research, 2020, 41(4): 381-394. doi: 10.24272/j.issn.2095-8137.2020.076
Citation: Qing-Bo Lu, Jian-Fei Sun, Qu-Yang Yang, Wen-Wen Cai, Meng-Qin Xia, Fang-Fang Wu, Ning Gu, Zhi-Jun Zhang. Magnetic brain stimulation using iron oxide nanoparticle-mediated selective treatment of the left prelimbic cortex as a novel strategy to rapidly improve depressive-like symptoms in mice. Zoological Research, 2020, 41(4): 381-394. doi: 10.24272/j.issn.2095-8137.2020.076

Magnetic brain stimulation using iron oxide nanoparticle-mediated selective treatment of the left prelimbic cortex as a novel strategy to rapidly improve depressive-like symptoms in mice

doi: 10.24272/j.issn.2095-8137.2020.076
#Authors contributed equally to this work
Funds:  This work was supported by grants from National Natural Science Foundation of China (81830040 to Z.J.Z.), National Key Projects for Research and Development Program of China (2016YFC1306700 to Z.J.Z., 2017YFA0104302 to N.G., and 2017YFA0104301 to J.F.S.), and Program of Excellent Talents in Medical Science of Jiangsu Province (JCRCA2016006 to Z.J.Z.)
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  • Magnetic brain stimulation has greatly contributed to the advancement of neuroscience. However, challenges remain in the power of penetration and precision of magnetic stimulation, especially in small animals. Here, a novel combined magnetic stimulation system (c-MSS) was established for brain stimulation in mice. The c-MSS uses a mild magnetic pulse sequence and injection of superparamagnetic iron oxide (SPIO) nanodrugs to elevate local cortical susceptibility. After imaging of the SPIO nanoparticles in the left prelimbic (PrL) cortex in mice, we determined their safety and physical characteristics. Depressive-like behavior was established in mice using a chronic unpredictable mild stress (CUMS) model. SPIO nanodrugs were then delivered precisely to the left PrL cortex using in situ injection. A 0.1 T magnetic field (adjustable frequency) was used for magnetic stimulation (5 min/session, two sessions daily). Biomarkers representing therapeutic effects were measured before and after c-MSS intervention. Results showed that c-MSS rapidly improved depressive-like symptoms in CUMS mice after stimulation with a 10 Hz field for 5 d, combined with increased brain-derived neurotrophic factor (BDNF) and inactivation of hypothalamic-pituitary-adrenal (HPA) axis function, which enhanced neuronal activity due to SPIO nanoparticle-mediated effects. The c-MSS was safe and effective, representing a novel approach in the selective stimulation of arbitrary cortical targets in small animals, playing a bioelectric role in neural circuit regulation, including antidepressant effects in CUMS mice. This expands the potential applications of magnetic stimulation and progresses brain research towards clinical application.

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  • [1]
    Berlim MT, van den Eynde F, Jeff Daskalakis Z. 2013. Clinically meaningful efficacy and acceptability of low-frequency repetitive transcranial magnetic stimulation (rTMS) for treating primary major depression: a meta-analysis of randomized, double-blind and sham-controlled trials. Neuropsychopharmacology, 38(4): 543−551. doi:  10.1038/npp.2012.237
    [2]
    Berlim MT, van den Eynde F, Tovar-Perdomo S, Daskalakis ZJ. 2014. 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. doi:  10.1017/S0033291713000512
    [3]
    Bestmann S. 2008. The physiological basis of transcranial magnetic stimulation. Trends in Cognitive Sciences, 12(3): 81−83. doi:  10.1016/j.tics.2007.12.002
    [4]
    Chen R, Romero G, Christiansen MG, Mohr A, Anikeeva P. 2015. Wireless magnetothermal deep brain stimulation. Science, 347(6229): 1477−1480. doi:  10.1126/science.1261821
    [5]
    Diana M, Raij T, Melis M, Nummenmaa A, Leggio L, Bonci A. 2017. Rehabilitating the addicted brain with transcranial magnetic stimulation. Nature Reviews Neuroscience, 18(11): 685−693. doi:  10.1038/nrn.2017.113
    [6]
    Fang GX, Wang Y. 2018. Effects of rTMS on hippocampal endocannabinoids and depressive-like behaviors in adolescent rats. Neurochemical Research, 43(9): 1756−1765. doi:  10.1007/s11064-018-2591-y
    [7]
    GBD 2016 Disease and Injury Incidence and Prevalence Collaborators. 2017. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. The Lancet, 390(10100): 1211−1259. doi:  10.1016/S0140-6736(17)32154-2
    [8]
    George MS, Nahas Z, Molloy M, Speer AM, Oliver NC, Li XB, Arana GW, Risch SC, Ballenger JC. 2000. A controlled trial of daily left prefrontal cortex TMS for treating depression. Biological Psychiatry, 48(10): 962−970. doi:  10.1016/S0006-3223(00)01048-9
    [9]
    George MS, Post RM. 2011. Daily left prefrontal repetitive transcranial magnetic stimulation for acute treatment of medication-resistant depression. The American Journal of Psychiatry, 168(4): 356−364. doi:  10.1176/appi.ajp.2010.10060864
    [10]
    Ghosal S, Bang E, Yue WZ, Hare BD, Lepack AE, Girgenti MJ, Duman RS. 2018. Activity-dependent brain-derived neurotrophic factor release is required for the rapid antidepressant actions of scopolamine. Biological Psychiatry, 83(1): 29−37. doi:  10.1016/j.biopsych.2017.06.017
    [11]
    Guadagnin V, Parazzini M, Fiocchi S, Liorni I, Ravazzani P. 2016. Deep transcranial magnetic stimulation: modeling of different coil configurations. IEEE Transactions on Biomedical Engineering, 63(7): 1543−1550. doi:  10.1109/TBME.2015.2498646
    [12]
    Guduru R, Liang P, Hong J, Rodzinski A, Hadjikhani A, Horstmyer J, Levister E, Khizroev S. 2015. Magnetoelectric 'spin' on stimulating the brain. Nanomedicine, 10(13): 2051−2061. doi:  10.2217/nnm.15.52
    [13]
    Hadley D, Anderson BS, Borckardt JJ, Arana A, Li XB, Nahas Z, George MS. 2011. Safety, tolerability, and effectiveness of high doses of adjunctive daily left prefrontal repetitive transcranial magnetic stimulation for treatment-resistant depression in a clinical setting. The Journal of ECT, 27(1): 18−25. doi:  10.1097/YCT.0b013e3181ce1a8c
    [14]
    Hauer L, Sellner J, Brigo F, Trinka E, Sebastianelli L, Saltuari L, Versace V, Höller Y, Nardone R. 2019. Effects of repetitive transcranial magnetic stimulation over prefrontal cortex on attention in psychiatric disorders: a systematic review. Journal of Clinical Medicine, 8(4): 416. doi:  10.3390/jcm8040416
    [15]
    Herrera DG, Robertson HA. 1996. Activation of c-fos in the brain. Progress in Neurobiology, 50(2-3): 83−107. doi:  10.1016/S0301-0082(96)00021-4
    [16]
    Hesselberg ML, Wegener G, Buchholtz PE. 2016. Antidepressant efficacy of high and low frequency transcranial magnetic stimulation in the FSL/FRL genetic rat model of depression. Behavioural Brain Research, 314: 45−51. doi:  10.1016/j.bbr.2016.07.037
    [17]
    Huang H, Delikanli S, Zeng H, Ferkey DM, Pralle A. 2010. Remote control of ion channels and neurons through magnetic-field heating of nanoparticles. Nature Nanotechnology, 5(8): 602−606. doi:  10.1038/nnano.2010.125
    [18]
    Karege F, Bondolfi G, Gervasoni N, Schwald M, Aubry JM, Bertschy G. 2005. Low brain-derived neurotrophic factor (BDNF) levels in serum of depressed patients probably results from lowered platelet BDNF release unrelated to platelet reactivity. Biological Psychiatry, 57(9): 1068−1072. doi:  10.1016/j.biopsych.2005.01.008
    [19]
    Li K, Nejadnik H, Daldrup-Link HE. 2017. Next-generation superparamagnetic iron oxide nanoparticles for cancer theranostics. Drug Discovery Today, 22(9): 1421−1429. doi:  10.1016/j.drudis.2017.04.008
    [20]
    Li RR, Wang J, Yu XY, Xu PF, Zhang S, Xu JH, Bai YJ, Dai ZZ, Sun YX, Ye RD, Liu XF, Ruan G, Xu GL. 2019. Enhancing the effects of transcranial magnetic stimulation with intravenously injected magnetic nanoparticles. Biomaterials Science, 7(6): 2297−2307. doi:  10.1039/C9BM00178F
    [21]
    Loo CK, McFarquhar TF, Mitchell PB. 2008. A review of the safety of repetitive transcranial magnetic stimulation as a clinical treatment for depression. International Journal of Neuropsychopharmacology, 11(1): 131−147. doi:  10.1017/S1461145707007717
    [22]
    Luborzewski A, Schubert F, Seifert F, Danker-Hopfe H, Brakemeier EL, Schlattmann P, Anghelescu I, Colla M, Bajbouj M. 2007. Metabolic alterations in the dorsolateral prefrontal cortex after treatment with high-frequency repetitive transcranial magnetic stimulation in patients with unipolar major depression. Journal of Psychiatric Research, 41(7): 606−615. doi:  10.1016/j.jpsychires.2006.02.003
    [23]
    McGirr A, Karmani S, Arsappa R, Berlim MT, Thirthalli J, Muralidharan K, Yatham LN. 2016. Clinical efficacy and safety of repetitive transcranial magnetic stimulation in acute bipolar depression. World Psychiatry, 15(1): 85−86. doi:  10.1002/wps.20300
    [24]
    Meng QL, Cherry M, Refai A, Du XM, Lu HB, Hong E, Yang YH, Choa FS. 2018. Development of focused transcranial magnetic stimulation for rodents by copper-array shields. IEEE Transactions on Magnetics, 54(5): 9300504.
    [25]
    Molendijk ML, Spinhoven P, Polak M, Bus BAA, Penninx BWJH, Elzinga BM. 2014. Serum BDNF concentrations as peripheral manifestations of depression: evidence from a systematic review and meta-analyses on 179 associations (N=9484). Molecular Psychiatry, 19(7): 791−800. doi:  10.1038/mp.2013.105
    [26]
    Müller MB, Holsboer F. 2006. Mice with mutations in the HPA-system as models for symptoms of depression. Biological Psychiatry, 59(12): 1104−1115. doi:  10.1016/j.biopsych.2006.02.008
    [27]
    Oh H, Piantadosi SC, Rocco BR, Lewis DA, Watkins SC, Sibille E. 2019. The role of dendritic brain-derived neurotrophic factor transcripts on altered inhibitory circuitry in depression. Biological Psychiatry, 85(6): 517−526. doi:  10.1016/j.biopsych.2018.09.026
    [28]
    Otte C, Gold SM, Penninx BW, Pariante CM, Etkin A, Fava M, Mohr DC, Schatzberg AF. 2016. Major depressive disorder. Nature Reviews Disease Primers, 2: 16065. doi:  10.1038/nrdp.2016.65
    [29]
    Pariante CM, Lightman SL. 2008. The HPA axis in major depression: classical theories and new developments. Trends in Neurosciences, 31(9): 464−468. doi:  10.1016/j.tins.2008.06.006
    [30]
    Pascual-Leone A, Rubio B, Pallardó F, Catalá MD. 1996. Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression. The Lancet, 348(9022): 233−237. doi:  10.1016/S0140-6736(96)01219-6
    [31]
    Philip NS, Carpenter SL, Ridout SJ, Sanchez G, Albright SE, Tyrka AR, Price LH, Carpenter LL. 2015. 5 Hz Repetitive transcranial magnetic stimulation to left prefrontal cortex for major depression. Journal of Affective Disorders, 186: 13−17. doi:  10.1016/j.jad.2014.12.024
    [32]
    Polanía R, Nitsche MA, Ruff CC. 2018. Studying and modifying brain function with non-invasive brain stimulation. Nature Neuroscience, 21(2): 174−187. doi:  10.1038/s41593-017-0054-4
    [33]
    Roet M, Hescham SA, Jahanshahi A, Rutten BPF, Anikeeva PO, Temel Y. 2019. Progress in neuromodulation of the brain: a role for magnetic nanoparticles?. Progress in Neurobiology, 177: 1−14. doi:  10.1016/j.pneurobio.2019.03.002
    [34]
    Salvador R, Miranda PC. 2009. Transcranial magnetic stimulation of small animals: a modeling study of the influence of coil geometry, size and orientation. In: Proceedings of 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society. Minneapolis, MN, USA: IEEE, 2009: 674–677.
    [35]
    Stubbeman WF, Zarrabi B, Bastea S, Ragland V, Khairkhah R. 2018. Bilateral neuronavigated 20Hz theta burst TMS for treatment refractory depression: an open label study. Brain Stimulation, 11(4): 953−955. doi:  10.1016/j.brs.2018.04.012
    [36]
    Su TP, Huang CC, Wei IH. 2005. Add-on rTMS for medication-resistant depression: a randomized, double-blind, sham-controlled trial in Chinese patients. The Journal of Clinicalpsychiatry, 66(7): 930−937.
    [37]
    Sun JF, Zhang Y, Yang F, Ma M, Xiong F, Gu N. 2019. Research and development of medical magnetic nanomaterials. Science Bulletin, 64(8): 842−853.
    [38]
    Sun P, Wang FR, Wang L, Zhang Y, Yamamoto R, Sugai T, Zhang Q, Wang ZD, Kato N. 2011. Increase in cortical pyramidal cell excitability accompanies depression-like behavior in mice: a transcranial magnetic stimulation study. The Journal of Neuroscience, 31(45): 16464−16472. doi:  10.1523/JNEUROSCI.1542-11.2011
    [39]
    Tang AD, Lowe AS, Garrett AR, Woodward R, Bennett W, Canty AJ, Garry MI, Hinder MR, Summers JJ, Gersner R, Rotenberg A, Thickbroom G, Walton J, Rodger J. 2016. Construction and evaluation of rodent-specific rTMS coils. Frontiers in Neural Circuits, 10: 47.
    [40]
    Tarapore PE, Picht T, Bulubas L, Shin Y, Kulchytska N, Meyer B, Berger MS, Nagarajan SS, Krieg SM. 2016. Safety and tolerability of navigated TMS for preoperative mapping in neurosurgical patients. Clinical Neurophysiology, 127(3): 1895−1900. doi:  10.1016/j.clinph.2015.11.042
    [41]
    Trevizol AP, Blumberger DM. 2019. An update on repetitive transcranial magnetic stimulation for the treatment of major depressive disorder. Clinical Pharmacology and Therapeutics, 106(4): 747−762. doi:  10.1002/cpt.1550
    [42]
    Vertes RP. 2006. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience, 142(1): 1−20. doi:  10.1016/j.neuroscience.2006.06.027
    [43]
    Yue K, Guduru R, Hong J, Liang P, Nair M, Khizroev S. 2012. Magneto-electric nano-particles for non-invasive brain stimulation. PLoS One, 7(9): e44040. doi:  10.1371/journal.pone.0044040
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