Optimal deep brain stimulation of the subthalamic nucleus—a computational study
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Deep brain stimulation (DBS) of the subthalamic nucleus, typically with periodic, high frequency pulse trains, has proven to be an effective treatment for the motor symptoms of Parkinson’s disease (PD). Here, we use a biophysically-based model of spiking cells in the basal ganglia (Terman et al., Journal of Neuroscience, 22, 2963–976, 2002; Rubin and Terman, Journal of Computational Neuroscience, 16, 211–235, 2004) to provide computational evidence that alternative temporal patterns of DBS inputs might be equally effective as the standard high-frequency waveforms, but require lower amplitudes. Within this model, DBS performance is assessed in two ways. First, we determine the extent to which DBS causes Gpi (globus pallidus pars interna) synaptic outputs, which are burstlike and synchronized in the unstimulated Parkinsonian state, to cease their pathological modulation of simulated thalamocortical cells. Second, we evaluate how DBS affects the GPi cells’ auto- and cross-correlograms. In both cases, a nonlinear closed-loop learning algorithm identifies effective DBS inputs that are optimized to have minimal strength. The network dynamics that result differ from the regular, entrained firing which some previous studies have associated with conventional high-frequency DBS. This type of optimized solution is also found with heterogeneity in both the intrinsic network dynamics and the strength of DBS inputs received at various cells. Such alternative DBS inputs could potentially be identified, guided by the model-free learning algorithm, in experimental or eventual clinical settings.
- Benabid, A. (2003). Deep brain stimulation for Parkinson’s disease. Current Opinion in Neurobiology, 13, 696–706. CrossRef
- Benabid, A., Koudsie, A., Benazzouz, A., Piallat, B., Krack, P., Limousin-Dowsey, P., et al. (2001). Advances in neurology, Vol 86: Parkinson’s disease, chapter deep brain stimulation for Parkinson’s disease. Philadelphia: Lippincott Williams & Wilkins.
- Benazzouz, A., Gao, D., Ni, Z., Piallat, B., Bouali-Benazzouz, R., & Benabid, A. (2000). Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and the ventrolateral nucleus of the thalamus. Neuroscience, 99, 289–295. CrossRef
- Bergman, H., Feingold, A., Nini, A., Raz, A., Slovin, H., Abeles, M., et al. (1998). Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends in Neurosciences, 21, 32–38. CrossRef
- Beurrier, C., Bioulac, B., Audin, J., & Hammond, C. (2001). High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. Journal of Neurophysiology, 85, 1351–1356.
- Boraud, T., Bezard, E., Bioulac, B., & 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, 215, 17–20. CrossRef
- Deep Brain Stimulation for Parkinson’s Disease Study Group. (2001). Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson’s disease. New England Journal of Medicine, 345, 956–963. CrossRef
- Feng, X., Shea-Brown, E., Greenwald, B., Rabitz, H., & Kosut, R. (2007). Toward closed-loop optimization of deep brain stimulation for Parkinson’s disease: concepts and lessons from a computational model. Journal of Neural Engineering, 4(2), L14-L21. CrossRef
- Goldberg, D. (1989). Genetic algorithms in search, optimization and machine learning. Boston, MA.: Addison-Wesley.
- Hahn, P., Lee, D., Russo, G., Vitek, J., & McIntyre, C. (2005). Stimulation on a model of subthalamopallidal network activity. Society for Neuroscience Abstracts, 331.6.
- Hariz, M., Shamsgovara, P., Johansson, F., Hariz, G., & Fodstad, H. (1999). Tolerance and tremor rebound following long-term chronic thalamic stimulation for parkinsonian and essential tremor. Stereotactactic and Functional Neurosurgery, 72, 208–218. CrossRef
- Hashimoto, T., Elder, E., Okun, M., Patrick, S., & Vitek, J. (2003). Stimulation of the subthalaic nucleus changes the firing pattern of pallidal neurons. Journal of Neuroscience 23, 1916–1923.
- Hauptmann, C., Popovych, O. V., & Tass, P. A. (2005). Delayed feedback control of synchronization in locally coupled neuronal networks. Neurocomputing, 65, 759–767. CrossRef
- Kleiner-Fisman, G., Fisman, D. N., Sime, E., Saint-Cyr, J. A., Lozano, A. M., & Lang, A. E. (2003). Long-term of bilateral deep brain stimulation of the subthalamic nucleus in patients with advanced Parkinson’s disease. Jounal of Neurosurgery, 99, 489–495. CrossRef
- Krack, P., Batir, A., van Blercom, N., Chabardes, S., Fraix, V., Ardouin, C., et al. (2003). Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. New England Journal of Medicine, 349, 1925–1934. CrossRef
- Lyons, K., Koller, W., Wilkinson, S., & Pahwa, R. (2001). Long term safety and efficacy of unilateral deep brain stimulation of the thalamus for parkinsonian tremor. Journal of Neurology, Neurosurgery and Psychiatry, 71, 682–684. CrossRef
- Magnin, M., Morel, A., & Jeanmonod, D. (2000). Single-unit analysis of the pallidum, thalamus, and subthalamic nucleus in parkinsonian patients. Neuroscience, 96, 549–564. CrossRef
- Maurice, N., Thierry, A., Glowinski, J., & Deniau, J. (2003). Spontaneous and evoked activity of substantia nigra pars reticulata neurons during highfrequency stimulation of the subthalamic nucleus. Journal of Neuroscience, 23, 9929–9936.
- McIntyre, C. C., & Grill, W. M. (2002). Extracellular stimulation of central neurons: Influence of stimulus waveform and frequency on neuronal output. Journal of Neurophysiology, 88, 1592–1604.
- McIntyre, C., Grill, W., Sherman, D., & Thakor, N. V. (2004). Celluar effects of deep brain stimulation: Model-based study of activation and inhibition. Journal of Neurophysiology, 91, 1457–1469. CrossRef
- Montgomery, E., & Baker, K. (2000). Mechanisms of deep brain stimulation and future technical developments. Neurological Research, 22, 259–266.
- Nini, A., Feingold, A., Slovin, H., & Bergman, H. (1995). Neurons in the globus pallidus do not show correlated activity in the normal monkey, but phase-locked oscillations appear in the mptp model of parkinsonism. Journal Neurophysiology, 74, 1800–1805.
- Okun, M., Tagliati, M., Pourfar, M., Fernandez, H,. Rodriguez, R., Alterman, R., et al. (2005). Management of referred deep brain stimulation failures: A retrospective analysis from 2 movement disorders centers. Archives of Neurology, 62, 1250–1255. CrossRef
- Olanow, W., Brin, M., & Obeso, J. (2000). The role of deep brain stimulation as a surgical treatment for Parkinson’s disease. Neurology, 55(Supp.6):S60–S66.
- Popovych, O. V., Hauptmann, C., & Tass, P.A. (2005). Effective desynchronization by nonlinear delayed feedback. Physical Review Letters, 94, 164102-1-4. CrossRef
- Rizzone, M., Lanotte, M., Bergamasco, B., Tavella, A., Torre, E., Faccani, G., et al. (2001). Deep brain stimulation of the subthalamic nucleus in Parkinson’s disease: Effects of variation in stimulation parameters. Journal of Neurology, Neurosurgery and Psychiatry, 71, 215–219. CrossRef
- Rodriguez-Oroz, M. C., Obeso, J. A., Lang, A. E., Houeto, J. L., Pollak, P., et al. (2005). Bilateral deep brain stimulation in Parkinson’s disease: A multicentre study with 4 years follow-up. Brain, 128, 2240–2249. CrossRef
- Rodriguez-Oroz, M. C., Zamarbide, I., Guridi, J., Palmero, M. R., & Obeso, J. A. (2004). Efficacy of deep brain stimulation of the subthalamic nucleus in Parkinson’s disease 4 years after surgery: Double blind and open label evaluation. Journal of Neurology, Neurosurgery and Psychiatry, 75, 1382–1385. CrossRef
- Rosenblum, M., & Pikovsky, A. (2004). Delayed feedback control of collective synchrony: An approach to suppression of pathological brain rhythms. Physical Review E, 70, 041904-1-11. CrossRef
- Rubin, J., & Terman, D. (2004). High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. Journal of Computational Neuroscience, 16, 211–235. CrossRef
- Tass, P. A. (1999). Phase resetting in medicine and biology. Stochastic modeling and data analysis. Berlin: Springer.
- Tass, P. A. (2001). Desynchronizing double-pulse phase resetting and application to deep brain stimulation. Biological Cybernetics, 85, 343–354. CrossRef
- Tass, P. A. (2003). A model of desynchronizing deep brain stimulation with a demand-controlled coordinated reset of neural subpopulations. Biological Cybernetics, 89, 81–88. CrossRef
- Terman, D., Rubin, J., Yew, A., & Wilson, C. J. (2002). Activity patterns in a model for the subthalamopallidal network of the basal ganglia. Journal of Neuroscience, 22, 2963–2976.
- Windels, F., Bruet, N., Poupard, A., Urbain, N., Chouvet, G., Feuerstein, C., et al. (2000). Effects of high frequency stimulation of subthalamic nucleus on extracellular glutamate and gaba in substantia nigra and globus pallidus in the normal rat. European Journal of Neuroscience, 12, 4141–4146. CrossRef
- Optimal deep brain stimulation of the subthalamic nucleus—a computational study
Journal of Computational Neuroscience
Volume 23, Issue 3 , pp 265-282
- Cover Date
- Online ISSN
- Springer US
- Additional Links
- Deep brain stimulation
- Parkinson’s disease
- Basal ganglia
- Subthalamic nucleus
- Numerical optimization
- Neural network model
- Industry Sectors
- Author Affiliations
- 1. Department of Chemistry, Princeton University, Princeton, NJ, 08544, USA
- 2. Courant Institute of Mathematical Sciences and Center for Neural Science, New York University, 251 Mercer Street, New York, NY, 10012, USA
- 3. SC Solutions, Sunnyvale, CA, 94085, USA