The contribution of functional neurosurgery to the understanding of the physiopathology of Parkinson’s disease

DOI: 10.4236/apd.2013.23017   PDF   HTML   XML   3,853 Downloads   5,958 Views  


Functional neurosurgery is nowadays a recognized treatment for advanced Parkinson’s disease with pharmacologically uncontrolled symptoms. This procedure brings us the unique opportunity to deepen in the knowledge of PD’s physiopathology by recording patients’ neural activity, and possibly in the future it will let us select the appropriate target and the optimal chronic stimulation pattern.

Share and Cite:

Barcia, J. and Alonso-Frech, F. (2013) The contribution of functional neurosurgery to the understanding of the physiopathology of Parkinson’s disease. Advances in Parkinson's Disease, 2, 88-95. doi: 10.4236/apd.2013.23017.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Marttila, R.J. and Rinne, U.K. (1976) Epidemiology of Parkinson’s disease in Finland. Acta Neurologica Scandinavica, 53, 81-102. doi:10.1111/j.1600-0404.1976.tb04328.x
[2] Kuopio, A.M., Marttila, R.J., Helenius, H. and Rinne, U.K. (1999) Changing epidemiology of Parkinson’s disease in southwestern Finland. Neurology, 52, 302-308. doi:10.1212/WNL.52.2.302
[3] Forno, L.S. (1992) Neuropathologic features of Parkinson’s, Huntington’s, and Alzheimer’s diseases. Annals of the New York Academy of Sciences, 648, 6-16. doi:10.1111/j.1749-6632.1992.tb24519.x
[4] Silva, M.T. and Saphira, A.H.V. (2001) Parkinson’s disease En Mattson MP. Edit Pathogenensis of neurodegenerative disorders. Humana Press, Totowa, 53-79.
[5] Fahn, S., Libsch, L.R. and Cutler, R.W. (1971) Monoamines in the human neostriatum: Topographic distribution in normals and in Parkinson’s disease and their role in akinesia, rigidity, chorea, and tremor. Journal of the Neurological Sciences, 14, 427-455 doi:10.1016/0022-510X(71)90178-X
[6] Cotzias, G.C., Van Woert, M.H. and Schiffer, L.M. (1967) Aromatic amino acids and modification of Parkinsonism. The New England Journal of Medicine, 276, 374-379. doi:10.1056/NEJM196702162760703
[7] Yahr, M.D., Duvoisin, R.C., Schear, M.J., Barrett, R.E. and Hoehn, M.M. (1969) Treatment of Parkinsonism with levodopa. Archives of Neurology, 21, 343-354. doi:10.1001/archneur.1969.00480160015001
[8] Schrag, A., Ben-Shlomo, Y., Brown, R., Marsden, C.D. and Quinn, N. (1998) Young-onset Parkinson’s disease revisited clinical features, natural history, and mortality. Movement Disorders, 13, 885-894. doi:10.1002/mds.870130605
[9] Obeso, J.A., Grandas, F., Vaamonde, J., Luquin, M.R., Artieda, J., Lera, G., Rodríguez, M.C. and Martinez-Lage, J.M. (1989) Motor complications associated with chronic levodopa therapy in Parkinson’s disease. Neurology, 39, 11-19.
[10] Obeso, J.A., Rodríguez-Oroz, M.C., Chana, P., Lera, G., Rodríguez, M. And Olanow, C.W. (2000) The evolution and origin of motor complications in Parkinson’s disease. Neurology, 55, S13-S20.
[11] Obeso, J.A., Olanow, C.W. and Nutt, J.G. (2000) Levodopa motor complications in Parkinson’s disease. Trends in Neurosciences, 23, S2-S7. doi:10.1016/S1471-1931(00)00031-8
[12] Albin, R.L., Young, A.B. and Penney, J.B. (1989) The functional anatomy of basal ganglia disorders. Trends in Neurosciences, 12, 366-375. doi:10.1016/0166-2236(89)90074-X
[13] DeLong, M.R. (1990) Primate models of movement disorders of basal ganglia origin. Trends in Neurosciences, 13, 281-285. doi:10.1016/0166-2236(90)90110-V
[14] Obeso, J.A., Rodríguez, M.C. and DeLong, M.R. (1997) Surgery for Parkinson’s disease. Journal of Neurology, Neurosurgery & Psychiatry, 62, 2-8. doi:10.1136/jnnp.62.1.2
[15] Rodriguez, R.L., Fernandez, H.H., Haq, I. and Okun, M.S. (2007) Pearls in patient selection for deep brain stimulation. Neurologist, 13, 253-260. doi:10.1097/NRL.0b013e318095a4d5
[16] Bronstein, J.M., Tagliati, M., Alterman, R.L., Lozano, A.M., Volkmann, J., Stefani, A., Horak, F.B., Okun, M.S., Foote, K.D., Krack, P., Pahwa, R., Henderson, J.M., Hariz, M.I., Bakay, R.A., Rezai, A., Marks Jr., W.J., Moro, E., Vitek, J.L., Weaver, F.M., Gross, R.E. and DeLong, M.R. (2011) Deep brain stimulation for Parkinson disease: An expert consensus and review of key issues. Archives of Neurology, 68, 165. doi:10.1001/archneurol.2010.260
[17] Moro, E., Scerrati, M., Romito, L.M., Roselli, R., Tonali, P., Albanese, A. (1999) Chronic subthalamic nucleus stimulation reduces medication requirements in Parkinson’s disease. Neurology, 53, 85-90. doi:10.1212/WNL.53.1.85
[18] Magari?os-Ascone, C.M., Figueiras-Mendez, R., Riva-Meana, C. and Cordoba-Fernández, A. (2000) Subtha-lamic neuron activity related to tremor and movement in Parkinson’s disease. European Journal of Neuroscience, 12, 2597-2607. doi:10.1046/j.1460-9568.2000.00127.x
[19] Magnin, M., Morel, A. and Jeanmonod, D. (2000) Single-unit analysis of the pallidum, thalamus and subthalamic nucleus in parkinsonian patients. Neuroscience, 96, 549-564. doi:10.1016/S0306-4522(99)00583-7
[20] Hutchison, W.D., Allan, R.J., Opitz, H., Levy, R., Dostrovsky, J.O., Lang, A.E. and Lozano, A.M. (1998) Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson’s disease. Archives of Neurology, 44, 622-628.
[21] Rodríguez-Oroz, M.C., Rodríguez, M., Guridi, J., Mewes, K., Chockkman, V., Vitek, J., DeLong, M.R. and Obeso, J.A. (2001) The subthalamic nucleus in Parkinson’s disease: Somatotopic organization and physiological characteristics. Brain, 124, 1777-1790. doi:10.1093/brain/124.9.1777
[22] Schnitzler, A. and Gross, J. (2005) Normal and pathological oscillatory communication in the brain. Nature Reviews Neuroscience, 6, 285-296. doi:10.1038/nrn1650
[23] Brown, P., Oliviero, A., Mazzone, P., Insola, A., Tonali, P. and Di Lazzaro, V. (2001) Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease. The Journal of Neuroscience, 21, 1033.
[24] Brown, P. and Williams, D. (2005) Basal ganglia local field potential activity: Character and functional significance in the human. Clinical Neurophysiology, 116, 2510-2519. doi:10.1016/j.clinph.2005.05.009
[25] Priori, A., Foffani, G., Pesenti, A., Bianchi, A., Chiesa, V., Baselli, G., Caputo, E., Tamma, F., Rampini, P., Egidi, M., Locatelli, M., Barbieri, S. and Scarlato, G. (2002) Movement-related modulation of neural activity in human basal ganglia and its L-DOPA dependency: Recordings from deep brain stimulation electrodes in patients with Parkinson’s disease. Neurological Sciences, 23, S101-S102. doi:10.1007/s100720200089
[26] Priori, A., Foffani, G., Pesenti, A., Tamma, F., Bianchi, A.M., Pellegrini, M., Locatelli, M., Moxon, K.A. and Villani, R.M. (2004) Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson’s disease. Experimental Neurology, 189, 369. doi:10.1016/j.expneurol.2004.06.001
[27] Williams, D., Kühn, A., Kupsch, A., Tijssen, M., van Bruggen, G., Speelman, H., Hotton, G., Yarrow, K. and Brown, P. (2003) Behavioural cues are associated with modulations of synchronous oscillations in the human subthalamic nucleus. Brain, 126, 1975. doi:10.1093/brain/awg194
[28] Williams, D., Tijssen, M., Van Bruggen, G., Bosch, A., Insola, A., Di Lazzaro, V., Mazzone, P., Oliviero, A., Quartarone, A., Speelman, H. and Brown. P. (2002) Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain, 125, 1558-1569. doi:10.1093/brain/awg267
[29] Silberstein, P., Kühn, A.A., Kupsch, A., Trottenberg, T., Krauss, J., W?hrle, J.C., Mazzone, P., Insola, A., Di Lazzaro, V., Oliviero, A., Aziz, T. and Brown, P. (2003) Patterning of globus pallidus local field potentials differs between Parkinson’s disease and dystonia. Brain, 126, 2597. doi:10.1093/brain/awh106
[30] Kühn, A.A., Williams, D., Kupsch, A., Limousin, P., Hariz, M., Schneider, G.-H., Yarrow, K. and Brown, P. (2004) Event-related beta synchronization in human subthalamic nucleus correlates with motor performance. Brain, 127, 735.
[31] Fogelson, N., Kuhn, A.A., Silberstein, P., Limousin, P.D., Hariz, M., Trottenberg, T., Kupsch, A. and Brown, P. (2005) Frequency dependent effects of subthalamic nucleus stimulation in Parkinson’s disease. Neuroscience Letters, 382, 5-9. doi:10.1016/j.neulet.2005.02.050
[32] Alonso-Frech, F., Zamarbide, I., Alegre, M., Rodríguez-Oroz, M.C., Guridi, J., Manrique, M., Valencia, M., Artieda, J. and Obeso, J.A. (2006) Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson’s disease. Brain, 129, 1748-1757. doi:10.1093/brain/awl103
[33] Varela, F., Lachaux, J.P., Rodríguez, E. And Martinerie, J. (2001) The brainweb: Phase synchronization and largescale integration. Nature Reviews Neuroscience, 2, 229-239. doi:10.1038/35067550
[34] Challis, R.E. and Kitney, R.I. (1990) Biomedical signal processing (in four parts). Part 1. Time-domain methods. Medical & Biological Engineering & Computing, 28, 509-524. doi:10.1007/BF02442601
[35] Challis, R.E. and Kitney, R.I. (1991) Biomedical signal processing (in four parts). Part 3. The power spectrum and coherence function. Medical & Biological Engineering & Computing, 29, 225-241. doi:10.1007/BF02446704
[36] Levy, R., Ashby, P., Hutchinson, 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. doi:10.1093/brain/awf128
[37] Bergman, H., Feingold, A., Nini, A., Raz, A., Slovin, H., Abeles, M. and Vaadia, E. (1998) Physiological aspects of information processing in the basal ganglia of normal and Parkinsonian primates. Trends in Neurosciences, 21, 32-38. doi:10.1016/S0166-2236(97)01151-X
[38] Levy, R., Hutchison, W.D., Lozano, A.M. and Dostrovsky, J.O. (2002) Synchronized neuronal discharge in the basal ganglia of Parkinsonian patients is limited to oscillatory activity. The Journal of Neuroscience, 22, 2855-2861.
[39] Foffani, G., Ardolino, G., Meda, B., Egidi, M., Rampini, P., Caputo, E., Baselli, G. and Priori, A. (2005) Altered subthalamo-pallidal synchronisation in parkinsonian dyskinesias. Journal of Neurology, Neurosurgery and Psychiatry, 76, 426-428. doi:10.1136/jnnp.2004.043547
[40] Alegre, M., López-Azcárate, J., Alonso-Frech, F., Rodríguez-Oroz, M.C., Valencia, M., Guridi, J., Artieda, J. and Obeso, J.A. (2012) Subthalamic activity during diphasic dyskinesias in Parkinson’s disease. Movement Disorders, 27, 1178-1181. doi:10.1002/mds.25090
[41] Brown, P. (2003) Oscillatory nature of human basal ganglia activity: Relationship to the pathophysiology of Parkinson’s disease. Movement Disorders, 18, 357-363. doi:10.1002/mds.10358
[42] Eusebio, A. and Brown, P. (2007) Oscillatory activity in the basal ganglia. Parkinsonism & Related Disorders, 13, S434-S436. doi:10.1016/S1353-8020(08)70044-0
[43] Vorobyov, V.V., Schibaev, N.V., Morelli, M. and Carta, A.R. (2003) EEG modifications in the cortex and striatum after dopaminergic priming in the 6-hydroxydopamine rat model of Parkinson’s disease. Brain Research, 972, 177-185. doi:10.1016/S0006-8993(03)02528-9
[44] Berke, J.D., Okatan, M., Skurski, J. and Eichenbaum, H.B. (2004) Oscillatory entrainment of striatal neurons in freely moving rats. Neuron, 43, 883-896. doi:10.1016/j.neuron.2004.08.035
[45] Courtemanche, R., Fujii, N. and Graybiel, A.M. (2003) Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. The Journal of Neuroscience, 23, 11741-11752.
[46] Sochurkova, D. and Rektor, I. (2003) Event-related desynchronization/synchronization in the putamen. An SEEG case study. Experimental Brain Research, 149, 401-404.
[47] Steigerwald, F., P?tter, M., Herzog, J., Pinsker, M., Kopper, F., Mehdorn, H., Deuschl, G. and Volkmann, J. (2008) Neuronal activity of the human subthalamic nucleus in the parkinsonian and nonparkinsonian state. Journal of Neurophysiology, 100, 2515-2524. doi:10.1152/jn.90574.2008
[48] Kühn, A.A., Tsui, A., Aziz, T., Ray, N., Brücke, C., Kupsch, A., Schneider, G.H. and Brown, P. (2009) Pathological synchronisation in the subthalamic nucleus of patients with Parkinson’s disease relates to both bradykinesia and rigidity. Experimental Neurology, 215, 380-387. doi:10.1016/j.expneurol.2008.11.008
[49] Wingeier, B, Tcheng, T, Koop, M.M., Hill, B.C., Heit, G. and Bronte-Stewart, H.M. (2006) Intra-operative STN DBS attenuates the prominent beta rhythm in the STN in Parkinson’s disease. Experimental Neurology, 197, 244-251. doi:10.1016/j.expneurol.2005.09.016
[50] Bronte-Stewart, H., Barberini, C., Koop, M.M., et al. (2009) The STN beta-band profile in Parkinson’s disease is stationary and shows prolonged attenuation after deep brain stimulation. Experimental Neurology, 215, 20-28.
[51] Brown, P., Mazzone, P., Oliviero, A., et al. (2004) Effects of stimulation of the subthalamic area on oscillatory pallidal activity in Parkinson’s disease. Experimental Neurology, 188, 480-490.
[52] Kuhn, A.A., Kempf, F., Brucke, C., et al. (2008) High-frequency stimulation of the subthalamic nucleus suppresses oscillatory beta activity in patients with Parkinson’s disease in parallel with improvement in motor performance. The Journal of Neuroscience, 28, 6165-6173.
[53] Eusebio, A., Thevathasan, W., Doyle, G. L., Pogosyan, A., Bye, E., Foltynie, T., Zrinzo, L., Ashkan, K., Aziz, T. and Brown, P. (2011) Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients. Journal of Neurology, Neurosurgery and Psychiatry, 82, 569-573. doi:10.1136/jnnp.2010.217489
[54] Cassidy, M., Mazzone, P., Oliviero, A., Insola, A., Tonali, P., Di Lazzaro, V. and Brown, P. (2002) Movement related changes in synchronization in the human basal ganglia. Brain, 125, 1235-1246. doi:10.1093/brain/awf135
[55] Doyle, L.M., Kuhn, A.A., Hariz, M., Kupsch, A., Schneider, G.H. and Brown, P. (2005) Levodopa-induced modulation of subthalamic beta oscillations during selfpaced movements in patients with Parkinson’s disease. European Journal of Neuroscience, 21, 1403-1412. doi:10.1111/j.1460-9568.2005.03969.x
[56] Alegre, M., Alonso-Frech, F., Rodriguez-Oroz, M.C., Guridi, J., Zamarbide, I., Valencia, M., Manrique, M., Obeso, J.A. and Artieda, J. (2005) Movement-related changes in oscillatory activity in the human subthalamic nucleus: Ipsilateral vs. contralateral movements. European Journal of Neuroscience, 22, 2315-2324. doi:10.1111/j.1460-9568.2005.04409.x
[57] Paradiso, G., Saint-Cyr, J.A., Lozano, A.M., Lang, A.E. and Chen, R. (2003) Involvement of the human subthalamic nucleus in movement preparation. Neurology, 61, 1538-1545. doi:10.1212/01.WNL.0000096021.28967.57
[58] Chen, C.C., Litvak, V., Gilbertson, T., Kühn, A., Lu, C.S., Lee, S.T., Tsai, C.H., Tisch, S., Limousin, P., Hariz, M. and Brown, P. (2007) Excessive synchronization of basal ganglia neurons at 20 Hz slows movement in Parkinson’s disease. Experimental Neurology, 205, 214-221. doi:10.1016/j.expneurol.2007.01.027
[59] Obeso, J.A., Rodríguez-Oroz, M.C., Rodríguez, M., Lanciego, J.L., Artieda, J., Gonzalo, N. and Olanow, C.W. (2000) Pathophysiology of the basal ganglia in Parkinson’s disease. Trends in Neurosciences, 23, S8-S19. doi:10.1016/S1471-1931(00)00028-8
[60] Brown, P. and Eusebio, A. (2008) Paradoxes of functional neurosurgery: Clues from basal ganglia recordings. Movement Disorders, 23, 12-20. doi:10.1002/mds.21796
[61] Marsden, C.D. and Obeso, J.A. (1994) The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson’s disease. Brain, 117, 877-897. doi:10.1093/brain/117.4.877
[62] Kühn, A.A., Kupsch, A., Schneider, G.H. and Brown, P. (2006) Reduction in subthalamic 8-35 Hz oscillatory activity correlates with clinical improvement in Parkinson’s disease. European Journal of Neuroscience, 23, 1956-1960.
[63] Tsang, E.W., Hamani, C., Moro, E., Mazzella, F., Saha, U., Lozano, A.M., Hodaie, M., Chuang, R., Steeves, T., Lim, S.Y., Neagu, B. and Chen, R. (2012) Subthalamic deep brain stimulation at individualized frequencies for Parkinson disease. Neurology, 78, 1930-1938. doi:10.1212/WNL.0b013e318259e183
[64] Zaidel, A., Spivak, A., Grieb, B., Bergman, H. and Israel, Z. (2010) Subthalamic span of beta oscillations predicts deep brain stimulation efficacy for patients with Parkinson’s disease. Brain, 133, 2007-2021. doi:10.1093/brain/awq144
[65] Reck, C., Florin, E., Wojtecki, L., Krause, H., Groiss, S., Voges, J., Maarouf, M., Sturm, V., Schnitzler, A. and Timmermann, L. (2009) Characterisation of tremor-associated local field potentials in the subthalamic nucleus in Parkinson’s disease. European Journal of Neuroscience, 29, 599-612.

comments powered by Disqus

Copyright © 2020 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.