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Combination of Transcranial Electro-Acupuncture and Fermented Scutellaria baicalensis Ameliorates Motor Recovery and Cortical Neural Excitability Following Focal Stroke in Rats

경두개 전침과 발효황금 병행 투여가 흰쥐의 허혈성 뇌세포 손상에 미치는 효과

  • Kim, Min Sun (Department of Physiology, Wonkwang University School of Medicine) ;
  • Koo, Ho (Department of Physiology, Wonkwang University School of Medicine) ;
  • Choi, Myung Ae (Department of Physiology, Wonkwang University School of Medicine) ;
  • Moon, Se Jin (Department of Physiology, Wonkwang University School of Medicine) ;
  • Yang, Seung Bum (Department of Medical Non-commissioned Officer, Wonkwang Health Science University) ;
  • Kim, Jae-Hyo (Department of Meridian & Acupoint, College of Korean Medicine, Wonkwang University)
  • 김민선 (원광대학교 의과대학 생리학교실) ;
  • 구호 (원광대학교 의과대학 생리학교실) ;
  • 최명애 (원광대학교 의과대학 생리학교실) ;
  • 문세진 (원광대학교 의과대학 생리학교실) ;
  • 양승범 (원광보건대학교 의무부사관과) ;
  • 김재효 (원광대학교 한의과대학 경혈학교실)
  • Received : 2018.11.23
  • Accepted : 2018.12.06
  • Published : 2018.12.27

Abstract

Objectives : Non-invasive transcranial electrical stimulation is one of therapeutic interventions to change in neural excitability of the cortex. Transcranial electro-acupuncture (TEA) can modulate brain functions through changes in cortical excitability as a model of non-invasive transcranial electrical stimulation. Some composites of fermented Scutellaria baicalenis (FSB) can activate intercellular signaling pathways for activation of brain-derived neurotrophic factor that is critical for formation of neural plasticity in stroke patients. This study was aimed at evaluation of combinatory treatment of TEA and FSB on behavior recovery and cortical neural excitability in rodent focal stroke model. Methods : Focal ischemic stroke was induced by photothrombotic injury to the motor cortex of adult rats. Application of TEA with 20 Hz and $200{\mu}A$ in combination with daily oral treatment of FBS was given to stroke animals for 3 weeks. Motor recovery was evaluated by rotating bean test and ladder working test. Electrical activity of cortical pyramidal neurons of stroke model was evaluated by using multi-channel extracellular recording technique and thallium autometallography. Results : Compared with control stroke group who did not receive any treatment, Combination of TEA and FSB treatment resulted in more rapid recovery of forelimb movement following focal stroke. This combination treatment also elicited increase in spontaneous firing rate of putative pyramidal neurons. Furthermore expression of metabolic marker for neural excitability was upregulated in peri-infract area under thallium autometallography. Conclusions : These results suggest that combination treatment of TEA and FSB can be a possible remedy for motor recovery in focal stroke.

Keywords

References

  1. Wang Xiaoming. Atlas of clinical anatomy and scalp acupuncture lines. Paju : Koonja. 2016 : 1-164.
  2. Ha Chi-Hong, Han Sang-Gyun, Cho Myung-Rae, Ryu Choong-Ryul, Lee Byung-Ryul. A clinical study on 29 cases with stroke treated by common acupuncture therapy and scalp acupuncture. The Journal of Korean Acupuncture and Moxibustion Society. 2001 ; 18(3) : 82-90.
  3. Schockert T, Schnitker R, Boroojerdi B, Smith IQ, Yamamoto T, Vietzhe K, et al. Cortical activation by Yamamoto new scalp acupuncture in the treatment of patients with a stroke: a sham-controlled study using functional MRI. Acu Med. 2010 ; 28(4) : 212-214. https://doi.org/10.1136/aim.2010.002683
  4. Wang WE, Xie CL, Zheng GQ. A systematic review and meta-analysis of Baihui (GV20)-based scalp acupuncture in experimental ischemic stroke. Sci Rep. 2014; 4: 3981. https://doi.org/10.1038/srep03981
  5. Zhang ZJ, Wang XM, McAlonan GM. Neural acupuncture unit: a new concept for interpreting effects and mechanisms of acupuncture. Evid Based Complement Alternat Med. 2012 ; Article ID 429412 : 1-23. https://doi.org/10.1155/2012/429412
  6. Park J, Gwak J, Cho S et al. Effects of head acupuncture versus upper and lower limbs acupuncture on signal activation of blood oxygen level dependent (BOLD) fMRI on the brain and somatosensory cortex. The Journal of Korean Acupuncture & Moxtibustion Society. 2008 ; 25(5) : 151-165.
  7. Boonzaier J, van Tilborg GAF, Neggers SFW, Dijkhuizen RM. Noninvasive Brain Stimulation to Enhance Functional Recovery After Stroke: Studies in Animal Models. Neurorehabil Neural Repair. 2018 ; 32(11) : 927-940. https://doi.org/10.1177/1545968318804425
  8. Reed T, Cohen Kadosh R. Transcranial electrical stimulation (tES) mechanisms and its effects on cortical excitability and connectivity. Journal of Inherited Metabolic Disease. 2018; 1-8. https://doi.org/10.1007/s10545-018-0181-4
  9. Jo AR. The effect of combined repetitive-transcranial magnetic stimulation and scalp acupuncture on neuromotor function in ischemic stroke rat model. Chonnam National Univerity. Master's Thesis. 2016 : 1-44.
  10. Zhao N, Zhang J, Qiu M et al. Scalp acupuncture plus low-frequency rTMS promotes repair of brain white matter tracts in stroke patients: A DTI study. 1. J Integr Neurosci. 2018 ; 17(1) : 61-69. https://doi.org/10.3233/jin-170043
  11. Fong SYK, Li C, Ho YC, Li R, Wang Q, Wong YC,et al. Brain Uptake of Bioactive Flavones in Scutellariae Radix and Its Relationship to Anxiolytic Effect in Mice. Mol Pharm. 2017 ; 14(9) : 2908-2916. https://doi.org/10.1021/acs.molpharmaceut.7b00029
  12. Xu C, Ji GE. Bioconversion of flavones during fermentation in milk containing Scutellaria baicalensis extract by Lactobacillus brevis. J Microbiol Biotechnol. 2013 ; 23(10) : 1422-1427. https://doi.org/10.4014/jmb.1305.05001
  13. Moosavi F, Hosseini R, Saso L, Firuzi O. Modulation of neurotrophic signaling pathways by polyphenols. 1. Drug Des Devel Ther. 2015 ; 10 : 23-42. https://doi.org/10.2147/dddt.s96936
  14. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. New York: Academic Press. 2007.
  15. Yang JH, Kim MS, Gong BM, Cybermedic Co. Method of preparing combined extract powder of fermented Scutellariae Radix and Gastrodiae Rhizoma from compounding solution of micro-organism and natural enzyme. 2016: Patent No. 10-1734022-0000.
  16. Voroslakos M, Takeuchi Y, Brinyiczki K, Zombori T, Oliva A, Fernandez-Ruiz A, et al. Direct effects of transcranial electric stimulation on brain circuits in rats and humans. Nat Commun. 2018 ; 9(1) : 483. https://doi.org/10.1038/s41467-018-02928-3
  17. Nitsche MA, Fricke K, Henschke U, Schlitterlau A, Liebetanz D, Lang N, et al. Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol. 2003 ; 553(Pt 1) : 293-301. https://doi.org/10.1113/jphysiol.2003.049916
  18. Maclellan CL, Grams J, Adams K, Colbourne F. Combined use of a cytoprotectant and rehabilitation therapy after severe intracerebral hemorrhage in rats. Brain Res. 2005 ; 1063(1) : 40-47. https://doi.org/10.1016/j.brainres.2005.09.027
  19. Goldschmidt J, Wanger T, Engelhorn A, Friedrich H, Happel M, Ilango A, et al. High-resolution mapping of neuronal activity using the lipophilic thallium chelate complex TlDDC: protocol and validation of the method. Neuroimage. 2010 ; 49(1) :303-315. https://doi.org/10.1016/j.neuroimage.2009.08.012
  20. Bartho P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsaki G. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol. 2004 ; 92(1) : 600-608. https://doi.org/10.1152/jn.01170.2003
  21. Lee SJ. Scalp acupuncture for stroke recovery: A systematic review and meta-analysis of randomized controlled trials. Pusan National University. Doctor of Philosophy's Thesis. 2016 : 1-47.
  22. Carmichael ST, Chesselet MF. Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adult. J Neurosci. 2002 ; 22(14) : 6062-6070. https://doi.org/10.1523/jneurosci.22-14-06062.2002
  23. Zhang X, Zhang RL, Zhang ZG, Chopp M. Measurement of neuronal activity of individual neurons after stroke in the rat using a microwire electrode array. Journal of Neuroscience Methods. 2007 ; 162(1-2) : 91-100. https://doi.org/10.1016/j.jneumeth.2006.12.012
  24. Tokuno T, Kataoka K, Asai T, Chichibu S, Kuroda R, Ioku M, et al. Functional changes in thalamic relay neurons after focal cerebral infarct: a study of unit recordings from VPL neurons after MCA occlusion in rats. J Cereb Blood Flow Metab. 1992 ; 12(6) : 954-61. https://doi.org/10.1038/jcbfm.1992.132
  25. Hakon J, Quattromani MJ, Sjolund C, Tomasevic G, Carey L, Lee JM. et al. Multisensory stimulation improves functional recovery and resting-state functional connectivity in the mouse brain after stroke. NeuroImage: Clinical. 2018 ; 17 : 717-730. https://doi.org/10.1016/j.nicl.2017.11.022
  26. Zhao LR, Risedal A, Wojcik A, Hejzlar J, Johansson BB, Kokaia Z. Enriched environment influences brain-derived neurotrophic factor levels in rat forebrain after focal stroke. Neuroscience Letters. 2001 ; 305(3) : 169-172. https://doi.org/10.1016/s0304-3940(01)01837-7
  27. Sun J, Ke Z, Yip SP, Hu XL, Zheng XX, Tong KY. Gradually increased training intensity benefits rehabilitation outcome after stroke by BDNF upregulation and stress suppression. BioMed Res Int. 2014 ; 2014 : 925762. https://doi.org/10.1155/2014/925762
  28. Clarkson AN, Overman JJ, Zhong S, Mueller R, Lynch G, Carmichael ST. AMPA receptor-induced local brain-derived neurotrophic factor signaling mediates motor recovery after stroke. J Neurosci. 2011 ; 31(10) : 3766-3775. https://doi.org/10.1523/jneurosci.5780-10.2011
  29. Yoon KJ, Oh BM, Kim DY. Functional improvement and neuroplastic effects of anodal transcranial direct current stimulation (tDCS) delivered 1 day vs. 1 week after cerebral ischemia in rats. Brain Res. 2012 ; 1452 : 61-72. https://doi.org/10.1016/j.brainres.2012.02.062
  30. Kim MS, Koo H, Han SW, Paulus W, Nitsche MA, Kim YH, et al. Repeated anodal transcranial direct current stimulation induces neural plasticity-associated gene expression in the rat cortex and hippocampus. Restor Neurol Neurosci. 2017 ; 35(2) : 137-146. https://doi.org/10.3233/rnn-160689
  31. Henrich-Noack P, Sergeeva EG, Sabel BA. Non-invasive electrical brain stimulation: from acute to late-stage treatment of central nervous system damage. Neural Regen Res. 2017 ; 12(10) : 1590-1594. https://doi.org/10.4103/1673-5374.217322
  32. Liang W, Huang X, Chen W. The Effects of Baicalin and Baicalein on Cerebral Ischemia: A Review. Aging Dis. 2017 ; 8(6) : 850-867. https://doi.org/10.14336/ad.2017.0829
  33. Gasiorowski K, Lamer-Zarawska E, Leszek J, Parvathaneni K, Yendluri BB, Blach-Olszewska Z, et al. Flavones from root of Scutellaria baicalensis Georgi: drugs of the future in neurodegeneration? CNS Neurol Disord Drug Targets. 2011 ; 10(2) : 184-191. https://doi.org/10.2174/187152711794480384
  34. Bahn HJ, Jo JJ, Kim BH, et al. Effects of Scutellariae Radix on neuronal apoptosis of spinal cord contusion injury in rats. Journal of Korean Medicine Rehabilitation. 2011 ; 21(4) : 13-22.
  35. Chen J, Zhu RL, Nakayama M. Expression of the apoptosis-effector gene, BAX is upregulated in vulnerable hippocampal CA1 neurons following global ischemia. J Neurochem. 1996 ; 67 : 64-71.
  36. Gillardon F, Wickert H, Zimmermann M. Up-regulation of Bax and down-regulation of Bcl-2 is associated with kainate-induced apoptosis in mouse brain. Neurosci Lett. 1995 ; 192 : 85-88. https://doi.org/10.1016/0304-3940(95)11619-8
  37. Han JY, Kim JH, Park JH, Song MY, Song MK, Kim DJ, et al. Scalp acupuncture and electromagnetic convergence stimulation for patients with cerebral infarction: study protocol for a randomized controlled trial. Trials. 2016 ; 17 : 490. https://doi.org/10.1186/s13063-016-1611-y
  38. Wang G, Yu C, Li C, Tu S. Observations on the influence of skull acupuncture plus medication on serum MDA in acute cerebral infarcion patients. Shanghai Journal of Acupuncture and Moxibustion. 2009 ; 3 : 135-137.
  39. Sim KC, Kim GD, Kim KY, Chung HW, Kim GY. Effect of Sopung-tang and tDCS on motor functioin recovery and GDNF expression in phtothrombotic brain infarction induced rat model. Journal of Physiology & Pathology in Korean Medicine. 2012 ; 26(6) : 894-901.