Network perspectives on the mechanisms of deep brain stimulation

Neurobiology of Disease

Volumn 38, Issue 3, 2010, Pages 329-337

  McIntyre, Cameron C ^a   Hahn, Philip J ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Depression; Dystonia; Epilepsy; Essential Tremor; Neuromodulation; Neurostimulation; Obsessive Compulsive Disorder; Parkinson's Disease; Tourette's Syndrome

Indexed keywords

BASAL GANGLION; BRAIN BLOOD FLOW; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; BRAIN METABOLISM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; NERVE CELL NETWORK; NERVE PROJECTION; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REVIEW; SUBTHALAMIC NUCLEUS; THERAPY EFFECT;

ANIMALS; BRAIN; DEEP BRAIN STIMULATION; HUMANS; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; NEURONS;

EID: 77952544351     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.09.022     Document Type: Review

References (105)

1. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
2. Alexander G.E., Crutcher M.D., DeLong M.R. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. Prog. Brain Res. 1990, 85:119-146.
3. Anderson K.E., Mullins J. Behavioral changes associated with deep brain stimulation surgery for Parkinson's disease. Curr. Neurol. Neurosci. Rep. 2003, 3:306-313.
4. Arantes P.R., Cardoso E.F., Barreiros M.A., Teixeira M.J., Goncalves M.R., Barbosa E.R., Sukwinder S.S., Leite C.C., Amaro E. Performing functional magnetic resonance imaging in patients with Parkinson's disease treated with deep brain stimulation. Mov. Disord. 2006, 21:1154-1162.
5. Asanuma K., Tang C., Ma Y., Dhawan V., Mattis P., Edwards C., Kaplitt M.G., Feigin A., Eidelberg D. Network modulation in the treatment of Parkinson's disease. Brain 2006, 129:2667-2678.
6. Ashby P., Kim Y.J., Kumar R., Lang A.E., Lozano A.M. Neurophysiological effects of stimulation through electrodes in the human subthalamic nucleus. Brain 1999, 122(Pt 10):1919-1931.
7. Baker, K.B., Zhang, J., Xu, W., Bynum, E., Minnich, J., Vitek, J.L., 2008. The effect of train rate and pattern on motor behavior during deep brain stimulation of the globus pallidus internus in a non-human primate model of Parkinson's disease. Soc. Neurosci. Abstr. 139.5, Washington, DC.
8. Benabid A.L., Pollak P., Louveau A., Henry S., de Rougemont J. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl. Neurophysiol. 1987, 50:344-346.
9. Benabid A.L., Pollak P., Gervason C., Hoffmann D., Gao D.M., Hommel M., Perret J.E., de Rougemont J. Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 1991, 337:403-406.
10. Benabid A.L., Pollak P., Gao D., Hoffmann D., Limousin P., Gay E., Payen I., Benazzouz A. Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J. Neurosurg. 1996, 84:203-214.
11. Bergman H., Wichmann T., Karmon B., DeLong M.R. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J. Neurophysiol. 1994, 72:507-520.
12. Birdno M.J., Cooper S.E., Rezai A.R., Grill W.M. Pulse-to-pulse changes in the frequency of deep brain stimulation affect tremor and modeled neuronal activity. J. Neurophysiol. 2007, 98:1675-1684.
13. Birdno M.J., Kuncel A.M., Dorval A.D., Turner D.A., Grill W.M. Tremor varies as a function of the temporal regularity of deep brain stimulation. NeuroReport 2008, 19:599-602.
14. Bronte-Stewart H., Barberini C., Koop M.M., Hill B.C., Henderson J.M., Wingeier B. The STN beta-band profile in Parkinson's disease is stationary and shows prolonged attenuation after deep brain stimulation. Exp. Neurol. 2009, 215:20-28.
15. Brown P. Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson's disease. Mov. Disord. 2003, 18:357-363.
16. Buzsáki G. Large-scale recording of neuronal ensembles. Nat. Neurosci. 2004, 7:446-451.
17. Cooper I.S., Upton A.R., Amin I. Reversibility of chronic neurologic deficits. Some effects of electrical stimulation of the thalamus and internal capsule in man. Appl. Neurophysiol. 1980, 43:244-258.
18. Courtemanche R., Fujii N., Graybiel A.M. Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. J. Neurosci. 2003, 23:11741-11752.
19. Cruz A.V., Mallet N., Magill P.J., Brown P., Averbeck B.B. Effects of dopamine depletion on network entropy in the external globus pallidus. J. Neurophysiol. 2009, 102:1092-1102.
20. de Ruyter van Steveninck R.R., Lewen G.D., Strong S.P., Koberle R., Bialek W. Reproducibility and variability in neural spike trains. Science 1997, 275:1805-1808.
21. DeLong M.R., Wichmann T. Circuits and circuit disorders of the basal ganglia. Arch. Neurol. 2007, 64:20-24.
22. Devos D., Labyt E., Derambure P., Bourriez J.L., Cassim F., Reyns N., Blond S., Guieu J.D., Destée A., Defebvre L. Subthalamic nucleus stimulation modulates motor cortex oscillatory activity in Parkinson's disease. Brain 2004, 127:408-419.
23. Dorval A.D., Russo G.S., Hashimoto T., Xu W., Grill W.M., Vitek J.L. Deep brain stimulation reduces neuronal entropy in the MPTP-primate model of Parkinson's disease. J. Neurophysiol. 2008, 100:2807-2818.
24. Doyle L.M., Kuhn A.A., Hariz M., Kupsch A., Schneider G.H., Brown P. Levodopa-induced modulation of subthalamic beta oscillations during self-paced movements in patients with Parkinson's disease. Eur. J. Neurosci. 2005, 21:1403-1412.
25. Feng X.J., Greenwald B., Rabitz H., Shea-Brown E., Kosut R. Toward closed-loop optimization of deep brain stimulation for Parkinson's disease: concepts and lessons from a computational model. J. Neural Eng. 2007, 4:L14-21.
26. Foffani G., Priori A., Egidi M., Rampini P., Tamma F., Caputo E., Moxon K.A., Cerutti S., Barbieri S. 300-Hz subthalamic oscillations in Parkinson's disease. Brain 2003, 126:2153-2163.
27. Galati S., Mazzone P., Fedele E., Pisani A., Peppe A., Pierantozzi M., Brusa L., Tropepi D., Moschella V., Raiteri M., Stanzione P., Bernardi G., Stefani A. Biochemical and electrophysiological changes of substantia nigra pars reticulata driven by subthalamic stimulation in patients with Parkinson's disease. Eur. J. Neurosci. 2006, 23:2923-2928.
28. Gatev P., Wichmann T. Interactions between cortical rhythms and spiking activity of single basal ganglia neurons in the normal and parkinsonian state. Cereb. Cortex 2008, 19:1330-1344.
29. Goldberg J.A., Boraud T., Maraton S., Haber S.N., Vaadia E., Bergman H. Enhanced synchrony among primary motor cortex neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine primate model of Parkinson's disease. J. Neurosci. 2002, 22:4639-4653.
30. Goldberg J.A., Rokni U., Boraud T., Vaadia E., Bergman H. Spike synchronization in the cortex/basal-ganglia networks of Parkinsonian primates reflects global dynamics of the local field potentials. J. Neurosci. 2004, 24:6003-6010.
31. Goldberger A.L., Amaral L.A., Hausdorff J.M., Ivanov P., Peng C.K., Stanley H.E. Fractal dynamics in physiology: alterations with disease and aging. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(Suppl 1):2466-2472.
32. Gradinaru V., Mogri M., Thompson K.R., Henderson J.M., Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science 2009, 324:354-359.
33. Grafton S.T., Turner R.S., Desmurget M., Bakay R., Delong M., Vitek J., Crutcher M. Normalizing motor-related brain activity: subthalamic nucleus stimulation in Parkinson disease. Neurology 2006, 66:1192-1199.
34. Grill W.M., Snyder A.N., Miocinovic S. Deep brain stimulation creates an informational lesion of the stimulated nucleus. NeuroReport 2004, 15:1137-1140.
35. Guo Y., Rubin J.E., McIntyre C.C., Vitek J.L., Terman D. Thalamocortical relay fidelity varies across subthalamic nucleus deep brain stimulation protocols in a data-driven computational model. J. Neurophysiol. 2008, 99:1477-1492.
36. Hahn, P.J., Lee, D.C., Russo, G.S., Vitek, J.L., McIntyre, C.C., 2005. Effects of deep brain stimulation on a model of subthalamopallidal network activity. Soc. Neurosci. Abstr., 331.6, Washington D.C.
37. Hahn P.J., Russo G.S., Hashimoto T., Miocinovic S., Xu W., McIntyre C.C., Vitek J.L. Pallidal burst activity during therapeutic deep brain stimulation. Exp. Neurol. 2008, 211:243-251.
38. Hashimoto T., Elder C.M., Okun M.S., Patrick S.K., Vitek J.L. Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J. Neurosci. 2003, 23:1916-1923.
39. Hassler R., Riechert T., Mundinger F., Umbach W., Ganglberger J.A. Physiological observations in stereotaxic operations in extrapyramidal motor disturbances. Brain 1960, 83:337-350.
40. Hershey T., Revilla F.J., Wernle A.R., McGee-Minnich L., Antenor J.V., Videen T.O., Dowling J.L., Mink J.W., Perlmutter J.S. Cortical and subcortical blood flow effects of subthalamic nucleus stimulation in PD. Neurology 2003, 61:816-821.
41. Hilker R., Voges J., Weber T., Kracht L.W., Roggendorf J., Baudrexel S., Hoevels M., Sturm V., Heiss W.D. STN-DBS activates the target area in Parkinson disease: an FDG-PET study. Neurology 2008, 71:708-713.
42. Humphries M.D., Stewart R.D., Gurney K.N. A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J. Neurosci. 2006, 26:12921-12942.
43. Hutchison W.D., Dostrovsky J.O., Walters J.R., Courtemanche R., Boraud T., Goldberg J., Brown P. Neuronal oscillations in the basal ganglia and movement disorders: evidence from whole animal and human recordings. J. Neurosci. 2004, 24:9240-9243.
44. Jech R., Urgosik D., Tintera J., Nebuzelsky A., Krasensky J., Liscak R., Roth J., Ruzicka E. Functional magnetic resonance imaging during deep brain stimulation: a pilot study in four patients with Parkinson's disease. Mov. Disord. 2001, 16:1126-1132.
45. Johnson M.D., McIntyre C.C. Quantifying the neural elements activated and inhibited by globus pallidus deep brain stimulation. J. Neurophysiol. 2008, 100:2549-2563.
46. Johnson M.D., Miocinovic S., McIntyre C.C., Vitek J.L. Mechanisms and targets of deep brain stimulation in movement disorders. Neurotherapeutics 2008, 5:294-308.
47. Johnson M.D., Vitek J.L., McIntyre C.C. Pallidal stimulation that improves parkinsonian motor symptoms also modulates neuronal firing patterns in primary motor cortex in the MPTP-treated monkey. Exp. Neurol. 2009, 219:359-362.
48. Kaneoke Y., Vitek J.L. Burst and oscillation as disparate neuronal properties. J. Neurosci. Methods 1996, 68:211-223.
49. Karimi M., Golchin N., Tabbal S.D., Hershey T., Videen T.O., Wu J., Usche J.W., Revilla F.J., Hartlein J.M., Wernle A.R., Mink J.W., Perlmutter J.S. Subthalamic nucleus stimulation-induced regional blood flow responses correlate with improvement of motor signs in Parkinson disease. Brain 2008, 131:2710-2719.
50. Kelly R.M., Strick P.L. Macro-architecture of basal ganglia loops with the cerebral cortex: use of rabies virus to reveal multisynaptic circuits. Prog. Brain Res. 2004, 143:449-459.
51. Kita H., Tachibana Y., Nambu A., Chiken S. Balance of monosynaptic excitatory and disynaptic inhibitory responses of the globus pallidus induced after stimulation of the subthalamic nucleus in the monkey. J. Neurosci. 2005, 25:8611-8619.
52. Kuhn A.A., Kupsch A., Schneider G.H., Brown P. Reduction in subthalamic 8-35Hz oscillatory activity correlates with clinical improvement in Parkinson's disease. Eur. J. Neurosci. 2006, 23:1956-1960.
53. Kuhn A.A., Kempf F., Brucke C., Gaynor Doyle L., Martinez-Torres I., Pogosyan A., Trottenberg T., Kupsch A., Schneider G.H., Hariz M.I., Vandenberghe W., Nuttin B., Brown P. High-frequency stimulation of the subthalamic nucleus suppresses oscillatory beta activity in patients with Parkinson's disease in parallel with improvement in motor performance. J. Neurosci. 2008, 28:6165-6173.
54. Leblois A., Boraud T., Meissner W., Bergman H., Hansel D. Competition between feedback loops underlies normal and pathological dynamics in the basal ganglia. J. Neurosci. 2006, 26:3567-3583.
55. Lee K.H., Blaha C.D., Harris B.T., Cooper S., Hitti F.L., Leiter J.C., Roberts D.W., Kim U. Dopamine efflux in the rat striatum evoked by electrical stimulation of the subthalamic nucleus: potential mechanism of action in Parkinson's disease. Eur. J. Neurosci. 2006, 23:1005-1014.
56. Li S., Arbuthnott G.W., Jutras M.J., Goldberg J.A., Jaeger D. Resonant antidromic cortical circuit activation as a consequence of high-frequency subthalamic deep-brain stimulation. J. Neurophysiol. 2007, 98:3525-3537.
57. Limousin P., Krack P., Pollak P., Benazzouz A., Ardouin C., Hoffmann D., Benabid A.L. Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N. Engl. J. Med. 1998, 339:1105-1111.
58. Lin T.P., Carbon M., Tang C., Mogilner A.Y., Sterio D., Beric A., Dhawan V., Eidelberg D. Metabolic correlates of subthalamic nucleus activity in Parkinson's disease. Brain 2008, 131:1373-1380.
59. Llinás R.R., Ribary U., Jeanmonod D., Kronberg E., Mitra P.P. Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:15222-15227.
60. Logothetis N.K., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
61. Lozano A.M., Dostrovsky J., Chen R., Ashby P. Deep brain stimulation for Parkinson's disease: disrupting the disruption. Lancet Neurol. 2002, 1:225-231.
62. Ma, Y., Wichmann, T., 2004. Disruption of motor performance by basal ganglia stimulation. Soc. Neurosci. Abstr. 416.2, San Diego, CA.
63. Mayberg H.S., Lozano A.M., Voon V., McNeely H.E., Seminowicz D., Hamani C., Schwalb J.M., Kennedy S.H. Deep brain stimulation for treatment-resistant depression. Neuron 2005, 45:651-660.
64. McIntyre C.C., Grill W.M., Sherman D.L., Thakor N.V. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J. Neurophysiol. 2004, 91:1457-1469.
65. McIntyre C.C., Mori S., Sherman D.L., Thakor N.V., Vitek J.L. Electric field and stimulating influence generated by deep brain stimulation of the subthalamic nucleus. Clin. Neurophysiol. 2004, 115:589-595.
66. McIntyre C.C., Savasta M., Kerkerian-Le Goff L., Vitek J.L. Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin. Neurophysiol. 2004, 115:1239-1248.
67. McIntyre C.C., Miocinovic S., Butson C.R. Computational analysis of deep brain stimulation. Expert Rev. Med. Devices 2007, 4:615-622.
68. McIntyre, C.C., Hahn, P.J., Lowe, M.J., Phillips, M.D., 2008. Integration of patient-specific network models and fMRI activation during deep brain stimulation. Soc. Neurosci. Abstr., 641.2, Washington, DC.
69. Mink J.W. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 1996, 50:381-425.
70. Miocinovic S., Parent M., Butson C.R., Hahn P.J., Russo G.S., Vitek J.L., McIntyre C.C. Computational analysis of subthalamic nucleus and lenticular fasciculus activation during therapeutic deep brain stimulation. J. Neurophysiol. 2006, 96:1569-1580.
71. Montgomery E.B. Effects of GPi stimulation on human thalamic neuronal activity. Clin. Neurophysiol. 2006, 117:2691-2702.
72. Montgomery E.B. Basal ganglia physiology and pathophysiology: a reappraisal. Parkinsonism Relat. Disord. 2007, 13:455-465.
73. Montgomery E.B., Baker K.B. Mechanisms of deep brain stimulation and future technical developments. Neurol. Res. 2000, 22:259-266.
74. Montgomery E.B., Gale J.T. Mechanisms of action of deep brain stimulation(DBS). Neurosci. Biobehav. Rev. 2008, 32:388-407.
75. Nambu A. A new dynamic model of the cortico-basal ganglia loop. Prog. Brain Res. 2004, 143:461-466.
76. Nambu A., Tokuno H., Hamada I., Kita H., Imanishi M., Akazawa T., Ikeuchi Y., Hasegawa N. Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J. Neurophysiol. 2000, 84:289-300.
77. Pahapill P.A., Lozano A.M. The pedunculopontine nucleus and Parkinson's disease. Brain 2000, 123:1767-1783.
78. Parent A., Hazrati L.N. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Brain Res. Rev. 1995, 20:91-127.
79. Parent A., Hazrati L.N. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res. Brain Res. Rev. 1995, 20:128-154.
80. Payoux P., Remy P., Damier P., Miloudi M., Loubinoux I., Pidoux B., Gaura V., Rascol O., Samson Y., Agid Y. Subthalamic nucleus stimulation reduces abnormal motor cortical overactivity in Parkinson disease. Arch. Neurol. 2004, 61:1307-1313.
81. Perlmutter J.S., Mink J.W. Deep brain stimulation. Annu. Rev. Neurosci. 2006, 29:229-257.
82. Pessiglione M., Guehl D., Rolland A.S., Francois C., Hirsch E.C., Feger J., Tremblay L. Thalamic neuronal activity in dopamine-depleted primates: evidence for a loss of functional segregation within basal ganglia circuits. J. Neurosci. 2005, 25:1523-1531.
83. Phillips M.D., Baker K.B., Lowe M.J., Tkach J.A., Cooper S.E., Kopell B.H., Rezai A.R. Parkinson disease: pattern of functional MR imaging activation during deep brain stimulation of subthalamic nucleus-initial experience. Radiology 2006, 239:209-216.
84. Pralong E., Debatisse D., Maeder M., Vingerhoets F., Ghika J., Villemure J.G. Effect of deep brain stimulation of GPI on neuronal activity of the thalamic nucleus ventralis oralis in a dystonic patient. Neurophysiol. Clin. 2003, 33:169-173.
85. Priori A., Foffani G., Pesenti A., Tamma F., Bianchi A.M., Pellegrini M., Locatelli M., Moxon K.A., Villani R.M. Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson's disease. Exp. Neurol. 2004, 189:369-379.
86. Rasouli G., Rasouli M., Lenz F.A., Verhagen L., Borrett D.S., Kwan H.C. Fractal characteristics of human Parkinsonian neuronal spike trains. Neuroscience 2006, 139:1153-1158.
87. Rauch S.L., Dougherty D.D., Malone D., Rezai A., Friehs G., Fischman A.J., Alpert N.M., Haber S.N., Stypulkowski P.H., Rise M.T., Rasmussen S.A., Greenberg B.D. A functional neuroimaging investigation of deep brain stimulation in patients with obsessive-compulsive disorder. J. Neurosurg. 2006, 104:558-565.
88. Ray N.J., Jenkinson N., Wang S., Holland P., Brittain J.S., Joint C., Stein J.F., Aziz T. 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. 2008, 213:108-113.
89. Rezai A.R., Lozano A.M., Crawley A.P., Joy M.L., Davis K.D., Kwan C.L., Dostrovsky J.O., Tasker R.R., Mikulis D.J. Thalamic stimulation and functional magnetic resonance imaging: localization of cortical and subcortical activation with implanted electrodes. Technical note. J. Neurosurg. 1999, 90:583-590.
90. Rodriguez M., Pereda E., Gonzalez J., Abdala P., Obeso J.A. Neuronal activity in the substantia nigra in the anaesthetized rat has fractal characteristics. Evidence for firing-code patterns in the basal ganglia. Exp. Brain Res. 2003, 151:167-172.
91. Rubchinsky L.L., Kopell N., Sigvardt K.A. Modeling facilitation and inhibition of competing motor programs in basal ganglia subthalamic nucleus-pallidal circuits. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:14427-14432.
92. Rubin J.E., Terman D. High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J. Comput. Neurosci. 2004, 16:211-235.
93. Shi L.H., Luo F., Woodward D.J., Chang J.Y. Basal ganglia neural responses during behaviorally effective deep brain stimulation of the subthalamic nucleus in rats performing a treadmill locomotion test. Synapse 2006, 59:445-457.
94. Shils J.L., Mei L.Z., Arle J.E. Modeling parkinsonian circuitry and the DBS electrode. II. Evaluation of a computer simulation model of the basal ganglia with and without subthalamic nucleus stimulation. Stereotact. Funct. Neurosurg. 2008, 86:16-29.
95. Smith Y., Bevan M.D., Shink E., Bolam J.P. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 1998, 86:353-387.
96. Starr P.A., Rau G.M., Davis V., Marks W.J., Ostrem J.L., Simmons D., Lindsey N., Turner R.S. Spontaneous pallidal neuronal activity in human dystonia: comparison with Parkinson's disease and normal macaque. J. Neurophysiol. 2005, 93:3165-3176.
97. Stefurak T., Mikulis D., Mayberg H., Lang A.E., Hevenor S., Pahapill P., Saint-Cyr J., Lozano A. Deep brain stimulation for Parkinson's disease dissociates mood and motor circuits: a functional MRI case study. Mov. Disord. 2003, 18:1508-1516.
98. Strogatz S.H. Nonlinear Dynamics And Chaos: With Applications To Physics, Biology, Chemistry, And Engineering 1994, Addison-Wesley, Reading, Mass.
99. Strong S.P., Koberle R., de Ruyter van Steveninck R.R., Bialek W. Entropy and information in neural spike trains. Phys. Rev. Lett. 1998, 80:197-200.
100. Tass P.A. A model of desynchronizing deep brain stimulation with a demand-controlled coordinated reset of neural subpopulations. Biol. Cybern. 2003, 89:81-88.
101. Trost M., Su S., Su P., Yen R.F., Tseng H.M., Barnes A., Ma Y., Eidelberg D. Network modulation by the subthalamic nucleus in the treatment of Parkinson's disease. NeuroImage 2006, 31:301-307.
102. Urbano F.J., Leznik E., Llinas R.R. Cortical activation patterns evoked by afferent axons stimuli at different frequencies: an in vitro voltage-sensitive dye imaging study. Thalamus Rel. Syst. 2002, 1:371-378.
103. Wichmann T., Soares J. 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. 2006, 95:2120-2133.
104. Wichmann T., Bergman H., Starr P.A., Subramanian T., Watts R.L., DeLong M.R. 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. 1999, 125:397-409.
105. Xu W., Russo G.S., Hashimoto T., Zhang J., Vitek J.L. Subthalamic nucleus stimulation modulates thalamic neuronal activity. J. Neurosci. 2008, 28:11916-11924.