Advertisement

Network Models of the Basal Ganglia in Parkinson’s Disease: Advances in Deep Brain Stimulation Through Model-Based Optimization

  • Karthik Kumaravelu
  • Warren M. GrillEmail author
Chapter
Part of the Springer Series in Cognitive and Neural Systems book series (SSCNS, volume 13)

Abstract

Parkinson’s disease (PD) is a movement disorder resulting from degeneration of dopaminergic neurons in the substantia nigra pars compacta. Electrical stimulation of the sub-cortical regions of the brain (basal ganglia – BG), also known as deep brain stimulation (DBS), is an effective therapy for the motor symptoms of PD. However, despite clear clinical benefits, the therapeutic mechanisms of DBS are not fully understood. Computational models of the BG play a vital role in investigation of the neural basis of PD and determining the therapeutic mechanisms of DBS. We review several conductance-based computational models of the BG published in the literature. First, we explain the different circuits within the BG network associated with movement control. Second, we provide insights gained from different computational models of the BG on the neural basis of PD and therapeutic mechanisms of DBS. Third, we discuss the functionality of these models to optimize DBS parameters. Finally, we present various opportunities available to optimize further DBS therapy by laying out the critical elements lacking in existing models.

Keywords

Basal ganglia network model Parkinson’s disease Deep brain stimulation Model-based optimization Subcortical lesion Subthalamic nucleus Movement disorders Computational neuroscience Globus pallidus 

Notes

Acknowledgments

This work was supported by a grant from the US National Institutes of Health (NIH R37 NS040894).

References

  1. 1.
    Adamchic I, Hauptmann C, Barnikol UB, Pawelczyk N, Popovych O, Barnikol TT, Silchenko A, Volkmann J, Deuschl G, Meissner WG (2014) Coordinated reset neuromodulation for Parkinson’s disease: proof-of-concept study. Mov Disord 29:1679–1684CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Agarwal R, Sarma SV (2012) The effects of DBS patterns on basal ganglia activity and thalamic relay. J Comput Neurosci 33:151–167CrossRefGoogle Scholar
  3. 3.
    Agid Y (1987) Biochemistry of neurotransmitters in Parkinson’s disease. Mov Disord 2:166–230Google Scholar
  4. 4.
    Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366–375CrossRefGoogle Scholar
  5. 5.
    Anderson D, Beecher G, Ba F (2017) Deep brain stimulation in Parkinson’s disease: new and emerging targets for refractory motor and nonmotor symptoms. Parkinson’s Dis 2017:5124328Google Scholar
  6. 6.
    Anderson ME, Postupna N, Ruffo M (2003) Effects of high-frequency stimulation in the internal globus pallidus on the activity of thalamic neurons in the awake monkey. J Neurophysiol 89:1150–1160CrossRefGoogle Scholar
  7. 7.
    Arefin MS (2012). Performance analysis of single-site and multiple-site deep brain stimulation in basal ganglia for Parkinson’s disease. In: Electrical & Computer Engineering (ICECE), 2012 7th international conference on IEEE, p 149–152Google Scholar
  8. 8.
    Ashkan K, Rogers P, Bergman H, Ughratdar I (2017) Insights into the mechanisms of deep brain stimulation. Nat Rev Neurol 13:548–554CrossRefGoogle Scholar
  9. 9.
    Baudrexel S, Witte T, Seifried C, von Wegner F, Beissner F, Klein JC, Steinmetz H, Deichmann R, Roeper J, Hilker R (2011) Resting state fMRI reveals increased subthalamic nucleus–motor cortex connectivity in Parkinson’s disease. NeuroImage 55:1728–1738CrossRefGoogle Scholar
  10. 10.
    Benabid A-L, Pollak P, Louveau A, Henry S, De Rougemont J (1987) Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Stereotact Funct Neurosurg 50:344–346CrossRefGoogle Scholar
  11. 11.
    Bergman H, Wichmann T, Karmon B, DeLong M (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72:507–520CrossRefGoogle Scholar
  12. 12.
    Beurrier C, Congar P, Bioulac B, Hammond C (1999) Subthalamic nucleus neurons switch from single-spike activity to burst-firing mode. J Neurosci 19:599–609CrossRefGoogle Scholar
  13. 13.
    Bezard E, Boraud T, Bioulac B, Gross CE (1999) Involvement of the subthalamic nucleus in glutamatergic compensatory mechanisms. Eur J Neurosci 11:2167–2170CrossRefGoogle Scholar
  14. 14.
    Bin-Mahfoodh M, Hamani C, Sime E, Lozano AM (2003) Longevity of batteries in internal pulse generators used for deep brain stimulation. Stereotact Funct Neurosurg 80:56–60CrossRefGoogle Scholar
  15. 15.
    Bolam J, Hanley J, Booth P, Bevan M (2000) Synaptic organisation of the basal ganglia. J Anat 196:527–542CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Brocker DT, Swan BD, So RQ, Turner DA, Gross RE, Grill WM (2017) Optimized temporal pattern of brain stimulation designed by computational evolution. Sci Transl Med 9:eaah3532CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Brocker DT, Swan BD, Turner DA, Gross RE, Tatter SB, Koop MM, Bronte-Stewart H, Grill WM (2013) Improved efficacy of temporally non-regular deep brain stimulation in Parkinson’s disease. Exp Neurol 239:60–67CrossRefGoogle Scholar
  18. 18.
    Bronte-Stewart H, Barberini C, Koop MM, Hill BC, Henderson JM, Wingeier B (2009) The STN beta-band profile in Parkinson’s disease is stationary and shows prolonged attenuation after deep brain stimulation. Exp Neurol 215:20–28CrossRefGoogle Scholar
  19. 19.
    Brown P (2003) Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson’s disease. Mov Disord 18:357–363CrossRefGoogle Scholar
  20. 20.
    Calabresi P, Picconi B, Tozzi A, Ghiglieri V, Di Filippo M (2014) Direct and indirect pathways of basal ganglia: a critical reappraisal. Nat Neurosci 17:1022–1030CrossRefGoogle Scholar
  21. 21.
    Cassar IR, Titus ND, Grill WM (2017) An improved genetic algorithm for designing optimal temporal patterns of neural stimulation. J Neural Eng 14:066013CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Cassidy M, Mazzone P, Oliviero A, Insola A, Tonali P, Lazzaro VD, Brown P (2002) Movement-related changes in synchronization in the human basal ganglia. Brain 125:1235–1246CrossRefGoogle Scholar
  23. 23.
    Chen Y, Wang J, Wei X, Deng B, Che Y (2011) Particle swarm optimization of periodic deep brain stimulation waveforms. In: Control Conference (CCC), 2011 30th Chinese IEEE, p 754–757Google Scholar
  24. 24.
    Chu H-Y, McIver EL, Kovaleski RF, Atherton JF, Bevan MD (2017) Loss of hyperdirect pathway cortico-subthalamic inputs following degeneration of midbrain dopamine neurons. Neuron 95:1306–1318. e1305CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Cui G, Jun SB, Jin X, Pham MD, Vogel SS, Lovinger DM, Costa RM (2013) Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494:238–242CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Daneshzand M, Faezipour M, Barkana BD (2017) Computational stimulation of the basal ganglia neurons with cost effective delayed Gaussian waveforms. Front Comput Neurosci 11:73CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Deuschl G, Schade-Brittinger C, Krack P, Volkmann J, Schäfer H, Bötzel K, Daniels C, Deutschländer A, Dillmann U, Eisner W (2006) A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med 355:896–908CrossRefGoogle Scholar
  28. 28.
    Dorval AD, Kuncel AM, Birdno MJ, Turner DA, Grill WM (2010) Deep brain stimulation alleviates parkinsonian bradykinesia by regularizing pallidal activity. J Neurophysiol 104:911–921CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Dunn EM, Lowery MM (2013) Simulation of PID control schemes for closed-loop deep brain stimulation. In: Neural Engineering (NER), 2013 6th international IEEE/EMBS conference on IEEE, p 1182–1185Google Scholar
  30. 30.
    Ebert M, Hauptmann C, Tass PA (2014) Coordinated reset stimulation in a large-scale model of the STN-GPe circuit. Front Comput Neurosci 8:154CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Fan D, Wang Q (2015) Improving desynchronization of parkinsonian neuronal network via triplet-structure coordinated reset stimulation. J Theor Biol 370:157–170CrossRefGoogle Scholar
  32. 32.
    Feng X-J, Shea-Brown E, Greenwald B, Kosut R, Rabitz H (2007) Optimal deep brain stimulation of the subthalamic nucleus—a computational study. J Comput Neurosci 23:265–282CrossRefGoogle Scholar
  33. 33.
    Filion M (1991) Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res 547:140–144CrossRefGoogle Scholar
  34. 34.
    Gerfen CR, Wilson CJ (1996) Chapter II: The basal ganglia. In: Swanson LW, Björklund A, Hokfelt T (eds) Handbook of chemical neuroanatomy, Vol. 12: Integrated systems of the CNS, Part III. Elsevier Science Publishers, New York, pp 371–468Google Scholar
  35. 35.
    Glynn G, Ahmad S (2002) Three-dimensional electrophysiological topography of the rat corticostriatal system. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 188:695–703CrossRefGoogle Scholar
  36. 36.
    Gorzelic P, Schiff S, Sinha A (2013) Model-based rational feedback controller design for closed-loop deep brain stimulation of Parkinson’s disease. J Neural Eng 10:026016CrossRefGoogle Scholar
  37. 37.
    Grill WM, Cantrell MB, Robertson MS (2008) Antidromic propagation of action potentials in branched axons: implications for the mechanisms of action of deep brain stimulation. J Comput Neurosci 24:81–93CrossRefGoogle Scholar
  38. 38.
    Group D-BSfPsDS (2001) Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson’s disease. N Engl J Med 2001:956–963Google Scholar
  39. 39.
    Guiot G, Brion S(1953) Traitement des mouvements anormaux par la coagulation pallidale-Technique et resultats. In: Revue Neurologique MASSON EDITEUR 120 BLVD SAINT-GERMAIN, 75280 PARIS 06, FRANCE, p 578–580Google Scholar
  40. 40.
    Guo Y, Rubin JE (2011) Multi-site stimulation of subthalamic nucleus diminishes thalamocortical relay errors in a biophysical network model. Neural Netw 24:602–616CrossRefGoogle Scholar
  41. 41.
    Guo Y, Rubin JE, McIntyre CC, Vitek JL, Terman D (2008) Thalamocortical relay fidelity varies across subthalamic nucleus deep brain stimulation protocols in a data-driven computational model. J Neurophysiol 99:1477–1492CrossRefGoogle Scholar
  42. 42.
    Hahn PJ, McIntyre CC (2010) Modeling shifts in the rate and pattern of subthalamopallidal network activity during deep brain stimulation. J Comput Neurosci 28:425–441CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Hashimoto T, Elder CM, Okun MS, Patrick SK, Vitek JL (2003) Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J Neurosci 23:1916–1923CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Hassani O-K, Mouroux M, Feger J (1996) Increased subthalamic neuronal activity after nigral dopaminergic lesion independent of disinhibition via the globus pallidus. Neuroscience 72:105–115CrossRefGoogle Scholar
  45. 45.
    Hassler R, Riechert T (1954) Indikationen und Lokalisationsmethode der gezielten Hirnoperationen. Nervenarzt 25:441–447PubMedGoogle Scholar
  46. 46.
    Hauptmann C, Tass PA (2010) Restoration of segregated, physiological neuronal connectivity by desynchronizing stimulation. J Neural Eng 7:056008CrossRefGoogle Scholar
  47. 47.
    Heimer G, Bar-Gad I, Goldberg JA, Bergman H (2002) Dopamine replacement therapy reverses abnormal synchronization of pallidal neurons in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine primate model of parkinsonism. J Neurosci 22:7850–7855CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Herrington TM, Cheng JJ, Eskandar EN (2016) Mechanisms of deep brain stimulation. J Neurophysiol 115:19–38CrossRefGoogle Scholar
  49. 49.
    Hollerman JR, Grace AA (1992) Subthalamic nucleus cell firing in the 6-OHDA-treated rat: basal activity and response to haloperidol. Brain Res 590:291–299CrossRefGoogle Scholar
  50. 50.
    Holt AB, Netoff TI (2014) Origins and suppression of oscillations in a computational model of Parkinson’s disease. J Comput Neurosci 37:505–521CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Holt AB, Wilson D, Shinn M, Moehlis J, Netoff TI (2016) Phasic burst stimulation: a closed-loop approach to tuning deep brain stimulation parameters for Parkinson’s disease. PLoS Comput Biol 12:e1005011CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Humphries MD, Stewart RD, Gurney KN (2006) A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J Neurosci 26:12921–12942CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Jankovic J, Rajput AH, McDermott MP, Perl DP (2000) The evolution of diagnosis in early Parkinson disease. Arch Neurol 57:369–372CrossRefGoogle Scholar
  54. 54.
    Kang G, Lowery MM (2013) Interaction of oscillations, and their suppression via deep brain stimulation, in a model of the cortico-basal ganglia network. IEEE Trans Neural Syst Rehabil Eng 21:244–253CrossRefGoogle Scholar
  55. 55.
    Kita H, Kita T (2011) Cortical stimulation evokes abnormal responses in the dopamine-depleted rat basal ganglia. J Neurosci 31:10311–10322CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, Koudsie A, Limousin PD, Benazzouz A, LeBas JF (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:1925–1934CrossRefGoogle Scholar
  57. 57.
    Kühn AA, Kempf F, Brücke C, Doyle LG, Martinez-Torres I, Pogosyan A, Trottenberg T, Kupsch A, Schneider G-H, Hariz MI (2008) High-frequency stimulation of the subthalamic nucleus suppresses oscillatory β activity in patients with Parkinson’s disease in parallel with improvement in motor performance. J Neurosci 28:6165–6173CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Kumaravelu K, Brocker DT, Grill WM (2016) A biophysical model of the cortex-basal ganglia-thalamus network in the 6-OHDA lesioned rat model of Parkinson’s disease. J Comput Neurosci 40:207–229CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Kuncel AM, Grill WM (2004) Selection of stimulus parameters for deep brain stimulation. Clin Neurophysiol 115:2431–2441CrossRefGoogle Scholar
  60. 60.
    Laitinen LV, Bergenheim AT, Hariz MI (1992) Leksell’s posteroventral pallidotomy in the treatment of Parkinson’s disease. J Neurosurg 76:53–61CrossRefGoogle Scholar
  61. 61.
    Levy R, Ashby P, Hutchison WD, Lang AE, Lozano AM, Dostrovsky JO (2002) Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson’s disease. Brain 125:1196–1209CrossRefGoogle Scholar
  62. 62.
    Limousin P, Krack P, Pollak P, Benazzouz A, Ardouin C, Hoffmann D, Benabid A-L (1998) Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 339:1105–1111CrossRefGoogle Scholar
  63. 63.
    Liu C, Wang J, Deng B, Wei X, Yu H, Li H, Fietkiewicz C, Loparo KA (2016) Closed-loop control of tremor-predominant parkinsonian state based on parameter estimation. IEEE Trans Neural Syst Rehabil Eng 24:1109–1121CrossRefGoogle Scholar
  64. 64.
    Liu C, Wang J, Li H, Lu M, Deng B, Yu H, Wei X, Fietkiewicz C, Loparo KA (2017) Closed-loop modulation of the pathological disorders of the basal ganglia network. IEEE Trans Neural Netw Learn Syst 28:371–382CrossRefGoogle Scholar
  65. 65.
    Lourens MA, Schwab BC, Nirody JA, Meijer HG, van Gils SA (2015) Exploiting pallidal plasticity for stimulation in Parkinson’s disease. J Neural Eng 12:026005CrossRefGoogle Scholar
  66. 66.
    Lozano AM, Lang AE, Galvez-Jimenez N, Miyasaki J, Duff J, Hutchison W, Dostrovsky JO (1995) Effect of GPi pallidotomy on motor function in Parkinson’s disease. Lancet 346:1383–1387CrossRefGoogle Scholar
  67. 67.
    Lysyansky B, Popovych OV, Tass PA (2013) Optimal number of stimulation contacts for coordinated reset neuromodulation. Front Neuroengineering 6:5CrossRefGoogle Scholar
  68. 68.
    Magill P, Bolam J, Bevan M (2001) Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus–globus pallidus network. Neuroscience 106:313–330CrossRefGoogle Scholar
  69. 69.
    Mallet N, Pogosyan A, Márton LF, Bolam JP, Brown P, Magill PJ (2008) Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. J Neurosci 28:14245–14258CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    McIntyre CC, Grill WM, Sherman DL, Thakor NV (2004) Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J Neurophysiol 91:1457–1469CrossRefGoogle Scholar
  71. 71.
    Meyers R (1942) Surgical interruption of the pallidofugal fibers. Its effect on the syndrome of paralysis agitans and technical considerations in its application. NY State J Med 42:317–325Google Scholar
  72. 72.
    Moran RJ, Mallet N, Litvak V, Dolan RJ, Magill PJ, Friston KJ, Brown P (2011) Alterations in brain connectivity underlying beta oscillations in parkinsonism. PLoS Comput Biol 7:e1002124CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Moro E, Esselink R, Xie J, Hommel M, Benabid A, Pollak P (2002) The impact on Parkinson’s disease of electrical parameter settings in STN stimulation. Neurology 59:706–713CrossRefGoogle Scholar
  74. 74.
    Nambu A, Tokuno H, Hamada I, Kita H, Imanishi M, Akazawa T, Ikeuchi Y, Hasegawa N (2000) Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J Neurophysiol 84:289–300CrossRefGoogle Scholar
  75. 75.
    Nambu A, Tokuno H, Takada M (2002) Functional significance of the cortico–subthalamo–pallidal ‘hyperdirect’ pathway. Neurosci Res 43:111–117CrossRefGoogle Scholar
  76. 76.
    Pan HS, Walters JR (1988) Unilateral lesion of the nigrostriatal pathway decreases the firing rate and alters the firing pattern of globus pallidus neurons in the rat. Synapse 2:650–656CrossRefGoogle Scholar
  77. 77.
    Pirini M, Rocchi L, Sensi M, Chiari L (2009) A computational modelling approach to investigate different targets in deep brain stimulation for Parkinson’s disease. J Comput Neurosci 26:91CrossRefGoogle Scholar
  78. 78.
    Plenz D, Kital ST (1999) A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400:677CrossRefGoogle Scholar
  79. 79.
    Popovych OV, Lysyansky B, Rosenblum M, Pikovsky A, Tass PA (2017) Pulsatile desynchronizing delayed feedback for closed-loop deep brain stimulation. PLoS One 12:e0173363CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Rajput A, Sitte H, Rajput A, Fenton M, Pifl C, Hornykiewicz O (2008) Globus pallidus dopamine and Parkinson motor subtypes clinical and brain biochemical correlation. Neurology 70:1403–1410CrossRefGoogle Scholar
  81. 81.
    Ray N, Jenkinson N, Wang S, Holland P, Brittain J, Joint C, Stein J, Aziz T (2008) Local field potential beta activity in the subthalamic nucleus of patients with Parkinson’s disease is associated with improvements in bradykinesia after dopamine and deep brain stimulation. Exp Neurol 213:108–113CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Rizzone M, Lanotte M, Bergamasco B, Tavella A, Torre E, Faccani G, Melcarne A, Lopiano L (2001) Deep brain stimulation of the subthalamic nucleus in Parkinson’s disease: effects of variation in stimulation parameters. J Neurol Neurosurg Psychiatry 71:215–219CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Rosa M, Arlotti M, Ardolino G, Cogiamanian F, Marceglia S, Di Fonzo A, Cortese F, Rampini PM, Priori A (2015) Adaptive deep brain stimulation in a freely moving parkinsonian patient. Mov Disord 30:1003–1005CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Rubin JE, Terman D (2004) High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J Comput Neurosci 16:211–235CrossRefGoogle Scholar
  85. 85.
    Smith Y, Beyan M, Shink E, Bolam J (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neurosci-Oxford 86:353–388CrossRefGoogle Scholar
  86. 86.
    So RQ, Kent AR, Grill WM (2012) Relative contributions of local cell and passing fiber activation and silencing to changes in thalamic fidelity during deep brain stimulation and lesioning: a computational modeling study. J Comput Neurosci 32:499–519CrossRefGoogle Scholar
  87. 87.
    Soares J, Kliem MA, Betarbet R, Greenamyre JT, Yamamoto B, Wichmann T (2004) Role of external pallidal segment in primate parkinsonism: comparison of the effects of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-induced parkinsonism and lesions of the external pallidal segment. J Neurosci 24:6417–6426CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Su F, Wang J, Deng B, Li H (2015a) Effects of deep brain stimulation amplitude on the basal-ganglia-thalamo-cortical network. In: Control and Decision Conference (CCDC), 2015 27th Chinese IEEE, p 4049–4053Google Scholar
  89. 89.
    Su F, Wang J, Deng B, Wei X-L, Chen Y-Y, Liu C, Li H-Y (2015b) Adaptive control of Parkinson’s state based on a nonlinear computational model with unknown parameters. Int J Neural Syst 25:1450030CrossRefGoogle Scholar
  90. 90.
    Summerson SR, Aazhang B, Kemere C (2015) Investigating irregularly patterned deep brain stimulation signal design using biophysical models. Front Comput Neurosci 9:78CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Tass PA, Qin L, Hauptmann C, Dovero S, Bezard E, Boraud T, Meissner WG (2012) Coordinated reset has sustained aftereffects in parkinsonian monkeys. Ann Neurol 72:816–820CrossRefGoogle Scholar
  92. 92.
    Terman D, Rubin JE, Yew A, Wilson C (2002) Activity patterns in a model for the subthalamopallidal network of the basal ganglia. J Neurosci 22:2963–2976CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Vila M, Perier C, Feger J, Yelnik J, Faucheux B, Ruberg M, Raisman-Vozari R, Agid Y, Hirsch E (2000) Evolution of changes in neuronal activity in the subthalamic nucleus of rats with unilateral lesion of the substantia nigra assessed by metabolic and electrophysiological measurements. Eur J Neurosci 12:337–344CrossRefGoogle Scholar
  94. 94.
    Wang J, Nebeck S, Muralidharan A, Johnson MD, Vitek JL, Baker KB (2016) Coordinated reset deep brain stimulation of subthalamic nucleus produces long-lasting, dose-dependent motor improvements in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine non-human primate model of parkinsonism. Brain Stimul 9:609–617CrossRefGoogle Scholar
  95. 95.
    Wang R, Wang J, Chen Y, Deng B, Wei X (2011) A new deep brain stimulation waveform based on PWM. In: Biomedical Engineering and Informatics (BMEI), 2011 4th international conference on IEEE, p 1815–1819Google Scholar
  96. 96.
    Weaver FM, Follett K, Stern M, Hur K, Harris C, Marks WJ, Rothlind J, Sagher O, Reda D, Moy CS (2009) Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA 301:63–73CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Wichmann T, Bergman H, Starr PA, Subramanian T, Watts RL, DeLong MR (1999) Comparison of MPTP-induced changes in spontaneous neuronal discharge in the internal pallidal segment and in the substantia nigra pars reticulata in primates. Exp Brain Res 125:397–409CrossRefGoogle Scholar
  98. 98.
    Wichmann T, Soares J (2006) Neuronal firing before and after burst discharges in the monkey basal ganglia is predictably patterned in the normal state and altered in parkinsonism. J Neurophysiol 95:2120–2133CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Biomedical EngineeringDuke UniversityDurhamUSA
  2. 2.Department of Electrical and Computer EngineeringDuke UniversityDurhamUSA
  3. 3.Department of NeurobiologyDuke UniversityDurhamUSA
  4. 4.Department of NeurosurgeryDuke UniversityDurhamUSA

Personalised recommendations