The mode of action of electrical high frequency stimulation

Miriam Kammerer, Jonas M. Hebel, Thomas J. Feuerstein

.

DOI: 10.4236/jbise.2010.310134                

Abstract

This article analyses, on the basis of the pathophysiological grounds of various syndromes treated with deep brain stimulation, whether there is a collective explanation of the mode of action of the applied regional stimulations with high frequencies (HFS). This proposed hypothesis assumes that HFS selectively releases GABA. The selective GABA re- lease can explain the efficacy and the side effects of HFS in the various target regions according to the maxim of the philosopher William of Ockham that the simplest explanation is probably the correct explanation.

Keywords

HFS, DBS, Parkinson’s disease, Essential tremor, Huntington’s disease, Depression

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Benabid, A.L., Pollak, P., Louveau, A., Henry, S. and Rougemont, J.D. (1987) Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Applied Neurophysiology, 50(1-6), 344-346.
[2]	Benabid, A.L., Chabarde, S., Mitrofanis, J. and Pollak, P. (2009) Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson disease. Lancet Neurology, 8(1), 67-81.
[3]	Beurrier, C., Bioulac, B., Audin, J. and Hammond, C. (2001) High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. Journal of Neurophysiology, 85(4), 1351-1356.
[4]	Anderson, M.E., Postupna, N. and Ruffo, M. (2003) Effects of high-frequency stimulation in the internal globus pallidus on the activity of thalamic neurons in the awake monkey. Journal of Neurophysiology, 89(2), 1150-1160.
[5]	Montgomery, E.B. and Baker, K.B. (2000) Mechanisms of deep brain stimulation and future technical developments. Neurological Research, 22(3), 259-266.
[6]	Levy, R., Ashby, P., Hutchison, W.D., Lang, A.E., Lozano, A.M. and Dostrovsky, J.O. (2002) Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson’s disease. Brain, 125, 1196-1209.
[7]	Meissner, W., Leblois, A., Hansel, D., Bioulac, B., Gross, C.E., Benazzouz, A. and Boraud T. (2005) Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain, 128, 2372-2382.
[8]	Dostrovsky, J.O. and Lozano, A.M. (2002) Mechanisms of deep brain stimulation. Movement Disorders, 17(3) S63-S68.
[9]	Garcia, L., Allesandro, G.D., Bioulac, B. and Hammond, C. (2005) High-frequency stimulation in Parkinson’s disease: More or less? Trends in Neuroscience, 28(4), 209-216.
[10]	Moro, E., Esselink, R.J., Xie, J., Hommel, M., Benabid, A.L. and Pollak, P. (2002) The impact on Parkinson’s disease of electrical parameter settings in STN stimulation. Neurology, 59(5), 706-713.
[11]	Rizzone, M., Lamotte, M., Bergamasco, B., Tavella, A., Torre, E., Faccani, G., Melcarne, A. and Lopiano, L. (2001) Deep brain stimulation if the subthalamic nucleus in Parkinson’s disease: Effects of variation in stimulation parameters. Journal of Neurology, Neurosurgery, and Psychiatry, 71(2), 215-219.
[12]	Benabid, A.L., Benazzous, A. and Pollak, P. (2002) Mechanisms of deep brain stimulation. Movement Disorders, 17(3), S73-S74.
[13]	Nowak, L.G. and Bullier, J. (1998) Axons, but not cell bodies, are activated by electrical stimulation in cortical grey matter. I. evidence from chronaxie measurements. Experimental Brain Research, 118(4), 477-488.
[14]	Holsheimer, J., Demeulemeester, H., Nuttin, B. and Sutter, P.D. (2000) Identification of the target neuronal elements in electrical deep brain stimulation. European Journal of Neuroscience, 12(12), 4573-4577.
[15]	Holsheimer, J., Dijkstra, E.A., Demeulemeester, H. and Nuttin, B. (2000) Chronaxie calculated from current-duration and voltage-duration data. Journal of Neuroscience Methods, 97(1), 45-50.
[16]	Feuerstein, T.J. (2009) Antiparkinsonmittel. Pharmako- therapie des morbus Parkinson. In: Aktories, K., F?rstermann, U., Hofmann, F., Starke, K., Eds., Allgemeine und Spezielle Pharmakologie and Toxikologie, Urban & Fischer, München, 299-305.
[17]	Mantovani, M., Moser, A., Haas, C.A., Zentner, J. and Feuerstein, T.J. (2009) GABAA autoreceptors enhance GABA release from human neocortex: towards a me- chanism for high-frequency stimulation (HFS) in brain? Naunyn-Schmiedeberg’s Archives of Pharmacology, 380 (1), 45-58.
[18]	Chang, S., Shon, Y.M., Agnesi, F. and Lee, K.H. (2009) Microthalamotomy effect during deep brain stimulation: Potential involvement of adenosine and glutamate efflux. Conference Proceedings: 31st Annual International Conference of the IEEE EMBS, 3294-3297.
[19]	Plaha, P., Shlomo, Y.B., Patel, N.K. and Gill, S.S. (2006) Stimulation of the caudal zona incerta is superior to stimulation of the subthalamic nucleus in improving contralateral Parkinsonism. Brain, 129, 1732-1747.
[20]	Moro, E., Scerrati, M., Romito, L.M., Roselli, R., Tonali, P. and Albanese, A. (1999) Chronic subthalamic nucleus stimulation reduces medication requirements in Parkinson’s disease. Neurology, 53(1), 85-91.
[21]	Krack, P., Pollak, P., Limousin, P., Hoffman, D., Xie, J., Benazzouz, A. and Benabid, A.L. (1998) Subthalamic nucleus or internal pallidal stimulation in young onset Parkinson’s disease. Brain, 121, pp. 451-457.
[22]	Limousin, P., Pollak, P., Hoffmann, D., Benazzouz, A., Perret, J.E. and Benabid, A.L. (1996) Abnormal involuntary movements induced by subthalamic nucleus stimulation in parkinsonian patients. Movement Disorders, 11(3), 231-235.
[23]	Plaha, P. and Gill, S.S. (2005) Bilateral deep brain stimulation of the pedunculopontine nucleus for Parkinson’s disease. Neuroreport, 16(17), 1883-1887.
[24]	Pereira, E.A., Muthusamy, K.A., Pennington, N.D., Joint, C.A. and Aziz, T.Z. (2008) Deep brain stimulation of the pedunculopontine nucleus in Parkinson’s disease. Preliminary experience at Oxford. British Journal of Neurosurgery, 22(1), S41-S44.
[25]	Nandi, D., Liu, X., Winter, J.L., Aziz, T.Z. and Stein, J.F. (2002) Deep brain stimulation of the pedunculopontine region in the normal non-human primate. Journal of Clinical Neuroscience, 9(2), 170-174.
[26]	Stefani, A., Lozano, A.M., Peppe, A., Stanzione, P., Galati, S., Tropepi, D., Pierantozzi, M., Brusa, L., Scarnati, E. and Mazzone, P. (2007) Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson’s disease. Brain, 130, 1596-1607.
[27]	Parent, M. and Parent, A. (2002) Axonal collateralization in primate basal ganglia and related thalamic nuclei. Thalamus & Related systems, 2(1), 71-86.
[28]	Sato, F., Lavallée, P., Lévesque, M. and Parent, A. (2000) Single-axon tracing study of neurons of the external segment of the globus pallidus in primate. Journal of Comparative Neurology, 417(1), 17-31.
[29]	Volkmann, J. (2004) Deep brain stimulation for the treatment of Parkinson’s disease. Journal of Clinical Neurophysiology, 21(1), 6-17.
[30]	Siegfried, J. and Lippitz, B. (1994) Bilateral chronic electrostimulation of ventroposterolateral pallidum: A new therapeutic approach for alleviating all parkinsonian symptoms. Neurosurgery, 35(6), 1126-1129.
[31]	Perlmutter, J.S. and Mink, J.W. (2006) Deep brain stimulation. Annual Review of Neuroscience, 29, 229-257.
[32]	Peppe, A., Pierantozzi, M., Altibrandi, M.G., Giacomini, P., Stefani, A., Bassi, A., Mazzone, P., Bernardi G. and Stanzione, P. (2001) Bilateral GPi DBS is useful to reduce abnormal involuntary movements in advanced Parkinson’s disease patients, but its action is related to modality and site of stimulation. European Journal of Neurology, 8 (6), 579-586.
[33]	Bejjani, B., Damier, P., Arnulf, I., Bonnet, A.M., Vidailhet, M., Dormont, D., Pidoux, B., Cornu, P., Marsault C. and Agid, Y. (1997) Pallidal stimulation for Parkinson’s disease. Two targets? Neurology, 49(6), 1564-9156.
[34]	Krack, P., Pollak, P., Limousin, P., Hoffman, D., Benazzouz A. and. Bas, J.F.L., Koudsie, A. and Benabid, A.L. (1998) Opposite motor effects of pallidal stimulation in Parkinson’s disease. Annals of Neurology, 43(2), 180-192.
[35]	Tronnier, V.M., Fogel, W., Kronenbuerger, M. and Steinvorth, S. (1997) Pallidal stimulation: an alternative to pallidotomy? Journal of Neurosurgery, 87(5), 700-705.
[36]	Papa, S.M., Desimone, R., Fiorani, M. and Oldfield, E.H. (1999) Internal global pallidus discharge is nearly suppressed during levodopa-induced dyskinesias. Annals of Neurology, 46(5), 732-738.
[37]	Mantovani, M., Velthoven, V.V., Fuellgraf, H., Feuerstein, T.J. and Moser, A. (2006) Neuronal electrical high frequency stimulation enhances GABA outflow from human neocortical slices. Neurochemistry International, 49(4), 347-350.
[38]	Boraud, T., Bezard, E., Bioulac, B. and Gross, C. (1996) High frequency stimulation of the internal Globus pallidus (GPi) simultaneously improves parkinsonian symptoms and reduces the firing frequency of GPi neurons in the MPTP-treated monkey. Neuroscience Letters, 210(1), 17-20.
[39]	Ogura, M., Nakao, N., Nakai, E., Uematsu, Y. and Itakura, T. (2004) The mechanism and effect of chronic electrical stimulation of the globus pallidus for treatment of Parkinson disease. Journal of Neurosurgery, 100(6), 997-1001.
[40]	Peppe, A., Gasbarra, A., Stefani, A., Chiavalon, C., Pierantozzi, M., Fermi, E., Stanzione, P., Caltagirone, C. and Mazzone, P. (2008) Deep brain stimulation of CM/PF of thalamus could be the new elective target for tremor in advanced Parkinson’s Disease? Parkinsonism & Related Disorders, 14(6), 501-504.
[41]	Krauss, J.K., Pohle, T., Weigel, R. and Burgunder, J.M. (2002) Deep brain stimulation of the centre median- parafascicular complex in patients with movement disorders. Journal of Neurology, Neurosurgery and Psychiatry, 72(4), 546-548.
[42]	Ohye, C. and Shibazak, T. (2001) Lesioning the thalamus for dyskinesia. Stereotactic and Functional Neurosurgery, 77(1-4), 33-39.
[43]	Pahapill, P.A., Levy, R., Dostrovsky, J.O., Davis, K.D., Rezai, A.R., Tasker, R.R. and Lozano, A.M. (1999) Tremor arrest with thalamic microinjections of muscimol in patients with essential tremor. Annals of Neurology, 46(2), 249-252.
[44]	Strafella, A., Ashby, P., Munz, M., Dostrovsky, J.O., Lozano, A.M. and Lang, A.E. (1997) Inhibition of voluntary activity by thalamic stimulation in humans: relevance for the control of tremor. Movement Disorders, 12(5), 727-737.
[45]	Moro, E., Lang, A.E., Strafella, A.P., Poon, Y.Y., Arango, P., Dagher, A., Hutchison, W.D. and Lozano, A.M. (2004) Bilateral globus pallidus stimulation for Huntington’s disease. Annals of Neurology, 56(2), 290-294.
[46]	Fasano, A., Mazzone, P., Piano, C., Quaranta, D., Soleti F. and Bentivoglio, A.R. (2008) GPi-DBS in Huntington’s disease: Results on motor function and cognition in a 72-year-old case. Movement Disorders, 23(9), 1289-1292.
[47]	Mayberg, H.S., Lozano, A.M., Voon, V., McNeely, H.E., Seminowicz, D., Hamani, C., Schwalb, J.M. and. Kennedy, S.H. (2005) Deep brain stimulation for treatment-resistant depression. Neuron, 45(5), 651-660.
[48]	Temel, Y., Boothman, L.J., Blokland, A., Magill, P.J., Steinbusch, H.W., Vandewalle, V.V. and Sharp, T. (2007) Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proceedings of the National Academy of Sciences of the United States of America, 104(43), 17087-17092.
[49]	Voon, V., Krack, P., Lang, A.E., Lozano, A.M., Dujardin, K., Schüpbach, M., Ambrosia, J.D., Thobois, S., Tamma, F., Herzog, J., Speelman, J.D., Samanta, J., Kubu, C., Rossignol, H., Poon, Y.Y., Cyr, J.A.S., Ardouin, C. and Moro, E., (2008) A multicentre study on suicide outcomes following subthalamic stimulation for Parkinson’s disease. Brain, 131, 2720-2728.
[50]	Ferraro, G., Montalbano, M.E., Sardo, P. and Grutta, V.L., (1996) Lateral habenular influence on dorsal raphe neurons. Brain Research Bulletin, 41(1), 47-52.
[51]	Smith, Y., Bevan, M.D., Shink, E. and Bolam, J.P. (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience, 86(2), 353-387.
[52]	Sartorius, A. and Henn, F.A. (2007) Deep brain stimulation of the lateral habenula in treatment resistent major depression. Medical Hypotheses, 69(6), 1305-1308.
[53]	Oroz, M.C.R., Obeso, J.A., Lang, A.E., Houeto, J.L., Pollak, P., Rehncrona, S., Kulisevsky, J., Albanese, A., Volkmann, J., Hariz, M.I., Quinn, N.P., Speelman, J.D., Guridi, J., Zamarbide, I., Gironell, A., Molet, J., Sedano, B. P., Pidoux, B., Bonnet, A.M., Agid, Y., Xie, J., Benabid, A.L., Lozano, A.M., Cyr, J.S., Romito, L., Contarino, M.F., Scerrati, M., Fraix, V. and Blercom, N.V. (2005) Bilateral deep brain stimulation in Parkinson’s disease: a multicentre study with 4 years follow-up. Brain, 128, 2
[54]	Servello, D., Porta, M., Sassi, M., Brambilla, A., Robertson, M.M., (2008) Deep brain stimulation in 18 patients with severe Gilles de la Tourette syndrome refractory to treatment: The surgery and stimulation. Journal of Neurology, Neurosurgery and Psychiatry, 79(2), 136-142.
[55]	Greenberg, B.D., Gabriels, L.A., Jr, D.A.M., Rezai, A.R., Friehs, G.M., Okun, M.S., Shapira, N.A., Foote, K.D., Cosyns, P.R., Kubu, C.S., Malloy, P.F., Salloway, S.P., Giftakis, J.E., Rise, M.T., Machado, A.G., Baker, K.B., Stypulkowski, P.H., Goodman, W.K., Rasmussen, S.A. and Nuttin, B.J. (2010) Deep brain stimulation of the ventral internal capsule/ventral striatum for obsessive-compulsive disorder: worldwide experience. Molecular Psychiatry, 15(1), 64-79.
[56]	Gubellini, P., Salin, P., Goff, L.K.L. and Baunez, C. (2009) Deep brain stimulation in neurological diseases and experimental models: from molecule to complex behaviour. Progress in Neurobiology, 89(1), 79-123.