Impedance detection of the electrical resistivity of the wound tissue around deep brain stimulation electrodes permits registration of the encapsulation process in a rat model

Badstübner, Kathrin; Stubbe, Marco; Kröger, Thomas; Mix, Eilhard; Gimsa, Jan

doi:10.5617/jeb.4086

Abstract

An animal model of deep brain stimulation (DBS) was used in in vivo studies of the encapsulation process of custom-made platinum/iridium microelectrodes in the subthalamic nucleus of hemiparkinsonian rats via electrical impedance spectroscopy. Two electrode types with 100-μm bared tips were used: i) a unipolar electrode with a 200-μm diameter and a subcutaneous gold wire counter electrode and ii) a bipolar electrode with two parallelshifted 125-μm wires. Miniaturized current-controlled pulse generators (130 Hz, 200 μA, 60 μs) enabled chronic DBS of the freely moving animals. A phenomenological electrical model enabled recalculation of the resistivity of the wound tissue around the electrodes from daily in vivo recordings of the electrode impedance over two weeks. In contrast to the commonly used 1 kHz impedance, the resistivity is independent of frequency, electrode properties, and current density. It represents the ionic DC properties of the tissue. Significant resistivity changes were detected with a characteristic decrease at approximately the 2nd day after implantation. The maximum resistivity was reached before electrical stimulation was initiated on the 8th day, which resulted in a decrease in resistivity. Compared with the unipolar electrodes, the bipolar electrodes exhibited an increased sensitivity for the tissue resistivity.

References

Krack P, Hariz MI, Baunez C, Guridi J, Obeso JA. Deep brain stimulation: from neurology to psychiatry? Trends Neurosci. 2010;33:474-84. https://doi.org/10.1016/j.tins.2010.07.002
Open DOI Search in Google Scholar Back to article
Weaver FM, Follett K, Stern M, Hur K, Harris C, Marks WJ, Jr., et al. Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. Jama. 2009;301:63-73. https://doi.org/10.1001/jama.2008.929
Open DOI Search in Google Scholar Back to article
Moro E, Lozano AM, Pollak P, Agid Y, Rehncrona S, Volkmann J, et al. Long-term results of a multicenter study on subthalamic and pallidal stimulation in Parkinson's disease. Mov Disord. 2010;25:578-86. https://doi.org/10.1002/mds.22735
Open DOI Search in Google Scholar Back to article
Pizzolato G, Mandat T. Deep brain stimulation for movement disorders. Front Integr Neurosci. 2012;6:2. https://doi.org/10.3389/fnint.2012.00002
Open DOI Search in Google Scholar Back to article
Gimsa U, Schreiber U, Habel B, Flehr J, van Rienen U, Gimsa J. Matching geometry and stimulation parameters of electrodes for deep brain stimulation experimentsnumerical considerations. J Neurosci Methods. 2006;150:212-27. https://doi.org/10.1016/j.jneumeth.2005.06.013
Open DOI Search in Google Scholar Back to article
Cheung T, Tagliati M. Deep brain stimulation: can we do it better? Clin Neurophysiol. 2010;121:1979-80. https://doi.org/10.1016/j.clinph.2010.05.024
Open DOI Search in Google Scholar Back to article
Okun MS, Gallo BV, Mandybur G, Jagid J, Foote KD, Revilla FJ, et al. Subthalamic deep brain stimulation with a constantcurrent device in Parkinson's disease: an open-label randomised controlled trial. Lancet Neurol. 2012;11:140-9. https://doi.org/10.1016/S1474-4422(11)70308-8
Search in Google Scholar Back to article
Gross RE, McDougal ME. Technological advances in the surgical treatment of movement disorders. Curr Neurol Neurosci Rep. 2013;13:371. https://doi.org/10.1007/s11910-013-0371-2
Search in Google Scholar Back to article
Lettieri C, Rinaldo S, Devigili G, Pisa F, Mucchiut M, Belgrado E, et al. Clinical outcome of deep brain stimulation for dystonia: constant-current or constant-voltage stimulation? A non-randomized study. Eur J Neurol. 2015;22:919-26. https://doi.org/10.1111/ene.12515
Open DOI Search in Google Scholar Back to article
Benazzouz A, Gao DM, Ni ZG, Piallat B, Bouali-Benazzouz R, Benabid AL. Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ventrolateral nucleus of the thalamus in the rat. Neurosci. 2000;99:289-95. https://doi.org/10.1016/S0306-4522(00)00199-8
Search in Google Scholar Back to article
Salin P, Manrique C, Forni C, Kerkerian-Le Goff L. Highfrequency stimulation of the subthalamic nucleus selectively reverses dopamine denervation-induced cellular defects in the output structures of the basal ganglia in the rat. J Neurosci. 2002;22:5137-48.
Search in Google Scholar Back to article
Bruet N, Windels F, Carcenac C, Feuerstein C, Bertrand A, Poupard A, et al. Neurochemical mechanisms induced by high frequency stimulation of the subthalamic nucleus: increase of extracellular striatal glutamate and GABA in normal and hemiparkinsonian rats. J Neuropathol Exp Neurol. 2003;62:1228-40. https://doi.org/10.1093/jnen/62.12.1228
Open DOI Search in Google Scholar Back to article
Windels F, Carcenac C, Poupard A, Savasta M. Pallidal origin of GABA release within the substantia nigra pars reticulata during high-frequency stimulation of the subthalamic nucleus. J Neurosci. 2005;25:5079-86. https://doi.org/10.1523/JNEUROSCI.0360-05.2005
Open DOI Search in Google Scholar Back to article
Boulet S, Lacombe E, Carcenac C, Feuerstein C, Sgambato-Faure V, Poupard A, et al. Subthalamic stimulation-induced forelimb dyskinesias are linked to an increase in glutamate levels in the substantia nigra pars reticulata. J Neurosci. 2006;26:10768-76. https://doi.org/10.1523/JNEUROSCI.3065-06.2006
Open DOI Search in Google Scholar Back to article
Schulte T, Brecht S, Herdegen T, Illert M, Mehdorn HM, Hamel W. Induction of immediate early gene expression by high-frequency stimulation of the subthalamic nucleus in rats. Neurosci. 2006;138:1377-85. https://doi.org/10.1016/j.neuroscience.2005.12.034
Open DOI Search in Google Scholar Back to article
Fang X, Sugiyama K, Akamine S, Namba H. Improvements in motor behavioral tests during deep brain stimulation of the subthalamic nucleus in rats with different degrees of unilateral parkinsonism. Brain research. 2006;1120:202-10. https://doi.org/10.1016/j.brainres.2006.08.073
Open DOI Search in Google Scholar Back to article
So RQ, McConnell GC, August AT, Grill WM. Characterizing effects of subthalamic nucleus deep brain stimulation on methamphetamine-induced circling behavior in hemiParkinsonian rats. IEEE Trans Neural Syst Rehabil Eng. 2012;20:626-35. https://doi.org/10.1109/TNSRE.2012.2197761
Open DOI Search in Google Scholar Back to article
Cooperrider J, Furmaga H, Plow E. Chronic deep cerebellar stimulation promotes long-term potentiation, microstructural plasticity, and reorganization of perilesional cortical representation in a rodent model. J Neurosci. 2014;34:9040-50. https://doi.org/10.1523/JNEUROSCI.0953-14.2014
Open DOI Search in Google Scholar Back to article
Liu HY, Jin J, Tang JS, Sun WX, Jia H, Yang XP, et al. Chronic deep brain stimulation in the rat nucleus accumbens and its effect on morphine reinforcement. Addiction biology. 2008;13:40-6. https://doi.org/10.1111/j.1369-1600.2007.00088.x
Open DOI Search in Google Scholar Back to article
Forni C, Mainard O, Melon C, Goguenheim D, Kerkerian-Le Goff L, Salin P. Portable microstimulator for chronic deep brain stimulation in freely moving rats. J Neurosci Methods. 2012;209:50-7. https://doi.org/10.1016/j.jneumeth.2012.05.027
Open DOI Search in Google Scholar Back to article
Harnack D, Meissner W, Paulat R, Hilgenfeld H, Müller WD, Winter C, Morgenstern R, Kupsch A. 2008. Continuous high-frequency stimulation in freely moving rats: development of an implantable microstimulation system. J Neurosci Methods 2008;167:278-291 https://doi.org/10.1016/j.jneumeth.2007.08.019
Open DOI Search in Google Scholar Back to article
Badstuebner K, Gimsa U, Weber I, Tuchscherer A, Gimsa J. Deep brain stimulation of hemiparkinsonian rats with unipolar and bipolar electrodes for up to 6 weeks – behavioral testing of freely moving animals. Parkinson’s Dis. 2017. (In press).
Search in Google Scholar Back to article
Ewing SG, Porr B, Riddell J, Winter C, Grace AA. SaBer DBS: a fully programmable, rechargeable, bilateral, chargebalanced preclinical microstimulator for long-term neural stimulation. J Neurosci Methods. 2013;213:228-35. https://doi.org/10.1016/j.jneumeth.2012.12.008
Open DOI Search in Google Scholar Back to article
Spieles-Engemann AL, Collier TJ, Sortwell CE. A functionally relevant and long-term model of deep brain stimulation of the rat subthalamic nucleus: advantages and considerations. European J Neurosci. 2010;32:1092-9. https://doi.org/10.1111/j.1460-9568.2010.07416.x
Open DOI Search in Google Scholar Back to article
Gubellini P, Kachidian P. Animal models of Parkinson's disease: An updated overview. Revue neurologique. 2015;171:750-61. https://doi.org/10.1016/j.neurol.2015.07.011
Open DOI Search in Google Scholar Back to article
Gimsa J, Habel B, Schreiber U, van Rienen U, Strauss U, Gimsa U. Choosing electrodes for deep brain stimulation experiments--electrochemical considerations. J Neurosci Methods. 2005;142:251-65. https://doi.org/10.1016/j.jneumeth.2004.09.001
Open DOI Search in Google Scholar Back to article
Herrington TM, Cheng JJ, Eskandar EN. Mechanisms of deep brain stimulation. J Neurophys. 2016;115:19-38. https://doi.org/10.1152/jn.00281.2015
Open DOI Search in Google Scholar Back to article
Ungerstedt U. 6-Hydroxy-dopamine induced degeneration of central monoamine neurons. Eur J Pharmacol. 1968;5:107-10. https://doi.org/10.1016/0014-2999(68)90164-7
Search in Google Scholar Back to article
Foster KR, Schwan HP. Dielectric properties of tissues. Handbook of biological effects of electromagnetic fields. 1995;2:25-102.
Search in Google Scholar Back to article
Kerner TE, Paulsen KD, Hartov A, Soho SK, Poplack SP. Electrical impedance spectroscopy of the breast: clinical imaging results in 26 subjects. IEEE Trans Med Imaging. 2002;21:638-45. https://doi.org/10.1109/TMI.2002.800606
Open DOI Search in Google Scholar Back to article
Adler A, Amyot R, Guardo R, Bates JH, Berthiaume Y. Monitoring changes in lung air and liquid volumes with electrical impedance tomography. J Appl Physiol. 1997;83:1762-7.
Search in Google Scholar Back to article
Lueck S, Reichert D, Pliquett U, Minor T, Preusse CJ. Bioelectric impedance of the neonatal heart during normothermic ischemia. Biomed Tech. 2013;58: Suppl. 1, Walter de Gruyter. Berlin, Boston. https://doi.org/10.1515/bmt-2013-4452
Search in Google Scholar Back to article
Lempka SF, Miocinovic S, Johnson MD, Vitek JL, McIntyre CC. In vivo impedance spectroscopy of deep brain stimulation electrodes. J Neural Eng. 2009;6:046001. https://doi.org/10.1088/1741-2560/6/4/046001
Search in Google Scholar Back to article
Badstübner K, Kröger T, Mix E, Gimsa U, Benecke R, Gimsa J. Electrical impedance properties of deep brain stimulation electrodes during long-term in-vivo stimulation in the Parkinson model of the rat. In: Gabriel J, Schier J, Van Huffel S, Conchon E, Correia C, Fred A, et al., editors. Biomedical Engineering Systems and Technologies. Springer. 2013;357 ISBN:978-3-642-38255-0. pp. 287–97.
Search in Google Scholar Back to article
Williams JC, Hippensteel JA, Dilgen J, Shain W, Kipke DR. Complex impedance spectroscopy for monitoring tissue responses to inserted neural implants. J Neural Eng. 2007;4:410-23. https://doi.org/10.1088/1741-2560/4/4/007
Search in Google Scholar Back to article
Duan YY, Clark GM, Cowan RS. A study of intra-cochlear electrodes and tissue interface by electrochemical impedance methods in vivo. Biomaterials. 2004;25:3813-28. https://doi.org/10.1016/j.biomaterials.2003.09.107
Open DOI Search in Google Scholar Back to article
Newbold C, Mergen S, Richardson R, Seligman P, Millard R, Cowan R, et al. Impedance changes in chronically implanted and stimulated cochlear implant electrodes. Cochlear Implants Int. 2014;15:191-9. https://doi.org/10.1179/1754762813Y.0000000050
Open DOI Search in Google Scholar Back to article
Grill WM, Mortimer JT. Electrical properties of implant encapsulation tissue. Ann Biomed Eng. 1994;22:23-33. https://doi.org/10.1007/BF02368219
Search in Google Scholar Back to article
Otto KJ, Johnson MD, Kipke DR. Voltage pulses change neural interface properties and improve unit recordings with chronically implanted microelectrodes. IEEE Trans Biomed Eng. 2006;53:333-40. https://doi.org/10.1109/TBME.2005.862530
Open DOI Search in Google Scholar Back to article
Charlet de Sauvage R, Lima da Costa D, Erre JP, Aran JM. Electrical and physiological changes during short-term and chronic electrical stimulation of the normal cochlea. Hear. Res. 1997;110:119-34. https://doi.org/10.1016/S0378-5955(97)00066-X
Search in Google Scholar Back to article
Lempka SF, Johnson MD, Moffitt MA, Otto KJ, Kipke DR, McIntyre CC. Theoretical analysis of intracortical microelectrode recordings. J Neural Eng. 2011;8:045006. https://doi.org/10.1088/1741-2560/8/4/045006
Search in Google Scholar Back to article
Abouzari MS, Berkemeier F, Schmitz G, Wilmer D. On the physical interpretation of constant phase elements. Solid State Ionics. 2009;180:922-7. https://doi.org/10.1016/j.ssi.2009.04.002
Open DOI Search in Google Scholar Back to article
Jorcin J-B, Orazem ME, Pébère N, Tribollet B. CPE analysis by local electrochemical impedance spectroscopy. Electrochimica Acta. 2006;51:1473-9. https://doi.org/10.1016/j.electacta.2005.02.128
Open DOI Search in Google Scholar Back to article
MacDonald JR. Impedence Spectroscopy - Emphasizing Solid Materials and Systems. Wiley. 1987:1-346.
Search in Google Scholar Back to article
Bisquert J, Garcia-Belmonte G, Bueno P, Longo E, Bulhoes L. Impedance of constant phase element (CPE)-blocked diffusion in film electrodes. J Neuropathol Exp Neurol. 1998;452:229-34. https://doi.org/10.1016/s0022-0728(98)00115-6
Search in Google Scholar Back to article
Conway BE, Bockris JO'M, White RE. Modern Aspects of Electrochemistry. Springer. 1999. ISBN:978-0306459641
Search in Google Scholar Back to article
Minnikanti S, Pereira MG, Jaraiedi S, Jackson K, Costa-Neto CM, Li Q, et al. In vivo electrochemical characterization and inflammatory response of multiwalled carbon nanotubebased electrodes in rat hippocampus. J Neural Eng. 2010;7:16002. https://doi.org/10.1088/1741-2560/7/1/016002
Search in Google Scholar Back to article
Nowak K, Mix E, Gimsa J, Strauss U, Sriperumbudur KK, Benecke R, et al. Optimizing a rodent model of Parkinson's disease for exploring the effects and mechanisms of deep brain stimulation. Parkinson’s Dis. 2011;2011:414682.
Search in Google Scholar Back to article
Asami K. Characterization of heterogeneous systems by dielectric spectroscopy. Progress in Polymer Science. 2002;27:1617-59. https://doi.org/10.1016/S0079-6700(02)00015-1
Search in Google Scholar Back to article
Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates, Sixth Edition: Hard Cover Edition. Academic Press. 2007. ISBN: 978-0125476126.
Search in Google Scholar Back to article
Ahmad Z. Polymeric dielectric materials, in Dielectric Material, ed. by Silaghi MA. InTech, Rijeka. 2012; 3-26.
Search in Google Scholar Back to article
Onaral B, Schwan H. Linear and nonlinear properties of platinum electrode polarisation. Part 1: frequency dependence at very low frequencies. Medical and biological engineering and computing. 1982;20:299-306. https://doi.org/10.1007/BF02442796
Search in Google Scholar Back to article
Gabriel S, Lau R, Gabriel C. The dielectric properties of biological tissues: II. Measurements in the frequency range 10 Hz to 20 GHz. Phys Med Biol. 1996;41:2251. https://doi.org/10.1088/0031-9155/41/11/002
Search in Google Scholar Back to article
Wintermantel E. Medizintechnik mit biokompatiblen Werkstoffen und Verfahren. Springer. 2002. ISBN:978-3540412618
Search in Google Scholar Back to article
Stubbe M, Gimsa J. Maxwell's mixing equation revisited: characteristic impedance equations for ellipsoidal cells. Biophys. J. 2015;109:194-208. https://doi.org/10.1016/j.bpj.2015.06.021
Open DOI Search in Google Scholar Back to article

Impedance detection of the electrical resistivity of the wound tissue around deep brain stimulation electrodes permits registration of the encapsulation process in a rat model

Abstract

Paradigm

My account