Neural origin of evoked potentials during thalamic deep brain stimulation

Journal of Neurophysiology

Volumn 110, Issue 4, 2013, Pages 826-843

  Kent, Alexander R ^a   Grill, Warren M ^a,b  

^a Duke University   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Computational model; Evoked compound action potential; Neural recording; Thalamus

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ISOFLURANE; LIDOCAINE; MUSCIMOL; TETRODOTOXIN;

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEPTH STIMULATION; CAT; COMPUTER SIMULATION; CONTROLLED STUDY; EVOKED RESPONSE; FEEDBACK SYSTEM; IN VIVO STUDY; LATERAL GENICULATE BODY; NONHUMAN; PRIORITY JOURNAL; THALAMUS; THALAMUS VENTRAL NUCLEUS;

EID: 84881629222     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00074.2013     Document Type: Article

References (98)

1. Anderson TR, Hu B, Iremonger K, Kiss ZH. Selective attenuation of afferent synaptic transmission as a mechanism of thalamic deep brain stimulation-induced tremor arrest. J Neurosci 26: 841850, 2006.
2. Ando N, Izawa Y, Shinoda Y. Relative contributions of thalamic reticular nucleus neurons and intrinsic interneurons to inhibition of thalamic neurons projecting to the motor cortex. J Neurophysiol 73: 2470-2485, 1995.
3. Baldissera F, Lundberg A, Udo M. Stimulation of preand postsynaptic elements in the red nucleus. Exp Brain Res 15: 151-167, 1972.
4. Balser JR, Nuss HB, Romashko DN, Marban E, Tomaselli GF. Functional consequences of lidocaine binding to slow-inactivated sodium channels. J Gen Physiol 107: 643-658, 1996.
5. Bedard C, Kroger H, Destexhe A. Model of low-pass filtering of local field potentials in brain tissue. Phys Rev E Stat Nonlin Soft Matter Phys 73: 051911, 2006.
6. Bedard C, Kroger H, Destexhe A. Modeling extracellular field potentials and the frequency-filtering properties of extracellular space. Biophys J 86: 1829-1842, 2004.
7. Benabid AL, Pollak P, Gervason C, Hoffmann D, Gao DM, Hommel M, Perret JE, de Rougemont J. Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 337: 403-406, 1991.
8. Benabid AL, Pollak P, Gross C, Hoffmann D, Benazzouz A, Gao DM, Laurent A, Gentil M, Perret J. Acute and long-term effects of subthalamic nucleus stimulation in Parkinson's disease. Stereotact Funct Neurosurg 62: 6-84, 1994.
9. Berkley KJ. Spatial relationships between the terminations of somatic sensory motor pathways in the rostral brainstem of cats and monkeys. II. Cerebellar projections compared with those of the ascending somatic sensory pathways in lateral diencephalon. J Comp Neurol 220: 229-251, 1983.
10. Birdno MJ, Grill WM. Mechanisms of deep brain stimulation in movement disorders as revealed by changes in stimulus frequency. Neurotherapeutics 5: 14-25, 2008.
11. Birdno MJ, Kuncel AM, Dorval AD, Turner DA, Gross RE, Grill WM. Stimulus features underlying reduced tremor suppression with temporally patterned deep brain stimulation. J Neurophysiol 107: 364-383, 2012.
12. Boehnke SE, Rasmusson DD. Time course and effective spread of lidocaine and tetrodotoxin delivered via microdialysis: an electrophysiological study in cerebral cortex. J Neurosci Methods 105: 133-141, 2001.
13. Boivie J. The termination of the spinothalamic tract in the cat. An experimental study with silver impregnation methods. Exp Brain Res 112: 331-353, 1971.
14. Briaire JJ, Frijns JH. Unraveling the electrically evoked compound action potential. Hear Res 205: 143-156, 2005.
15. Briggs F, Usrey WM. A fast, reciprocal pathway between the lateral geniculate nucleus and visual cortex in the macaque monkey. J Neurosci 27: 5431-5436, 2007.
16. Bronte-Stewart H, Barberini C, Koop MM, Hill BC, Henderson JM, Wingeier B. The STN beta-band profile in Parkinson's disease is stationary and shows prolonged attenuation after deep brain stimulation. Exp Neurol 215: 20-28, 2009.
17. Brown CJ, Abbas PJ. Electrically evoked whole-nerve action potentials: parametric data from the cat. J Acoust Soc Am 88: 2205-2210, 1990.
18. Brown P, Williams D. Basal ganglia local field potential activity: character and functional significance in the human. Clin Neurophysiol 116: 2510-2519, 2005.
19. Butler AB, Hodos W. Comparative Vertebrate Neuroanatomy: Evolution and Adaptation. Hoboken, NJ: Wiley, 2005.
20. Butson CR, McIntyre CC. Tissue and electrode capacitance reduce neural activation volumes during deep brain stimulation. Clin Neurophysiol 116: 2490-2500, 2005.
21. Cohen CJ, Bean BP, Colatsky TJ, Tsien RW. Tetrodotoxin block of sodium channels in rabbit Purkinje fibers. Interactions between toxin binding and channel gating. J Gen Physiol 78: 383-411, 1981.
22. Courtney KR. Mechanism of frequency-dependent inhibition of sodium currents in frog myelinated nerve by the lidocaine derivative GEA. J Pharmacol Exp Ther 195: 225-236, 1975.
23. Craig AD, Burton H. The distribution and topographical organization in the thalamus of anterogradely-transported horseradish peroxidase after spinal injections in cat and raccoon. Exp Brain Res 58: 227-254, 1985.
24. Detsch O, Kochs E, Siemers M, Bromm B, Vahle-Hinz C. Differential effects of isoflurane on excitatory and inhibitory synaptic inputs to thalamic neurones in vivo. Br J Anaesth 89: 294-300, 2002.
25. Deuschl G, Herzog J, Kleiner-Fisman G, Kubu C, Lozano AM, Lyons KE, Rodriguez-Oroz MC, Tamma F, Troster AI, Vitek JL, Volkmann J, Voon V. Deep brain stimulation: postoperative issues. Mov Disord 21, Suppl 14: S219-S237, 2006.
26. Eusebio A, Cagnan H, Brown P. Does suppression of oscillatory synchronisation mediate some of the therapeutic effects of DBS in patients with Parkinson's disease? Front Integr Neurosci 6: 47, 2012.
27. Frankemolle AM, Wu J, Noecker AM, Voelcker-Rehage C, Ho JC, Vitek JL, McIntyre CC, Alberts JL. Reversing cognitive-motor impairments in Parkinson's disease patients using a computational modelling approach to deep brain stimulation programming. Brain 133: 746-761, 2010.
28. Gold C, Henze DA, Koch C, Buzsaki G. On the origin of the extracellular action potential waveform: a modeling study. J Neurophysiol 95: 3113-3128, 2006.
29. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science 324: 354-359, 2009.
30. Grant PF, Lowery MM. Effect of dispersive conductivity and permittivity in volume conductor models of deep brain stimulation. IEEE Trans Biomed Eng 57: 2386-2393, 2010.
31. Helmholtz HL. Ueber einige Gesetze der vertheilung Elektrischer Ströme in korperlichen Leitern mit Anwendung auf die thierisch-electrischen Versuche. Ann Physik Chemie 89: 354-377, 1853.
32. Hersch SM, White EL. Thalamocortical synapses with corticothalamic projection neurons in mouse SmI cortex: electron microscopic demonstration of a monosynaptic feedback loop. Neurosci Lett 24: 207-210, 1981.
33. Hines ML, Carnevale NT. NEURON: a tool for neuroscientists. Neuroscientist 7: 123-135, 2001.
34. Hirai T, Jones EG. Segregation of lemniscal inputs and motor cortex outputs in cat ventral thalamic nuclei: application of a novel technique. Exp Brain Res 71: 329-344, 1988.
35. Hirai T, Ohye C, Nagaseki Y, Matsumura M. Cytometric analysis of the thalamic ventralis intermedius nucleus in humans. J Neurophysiol 61: 478-487, 1989.
36. Hodaie M, Wennberg RA, Dostrovsky JO, Lozano AM. Chronic anterior thalamus stimulation for intractable epilepsy. Epilepsia 43: 603-608, 2002.
37. Jeon EK, Brown CJ, Etler CP, O'Brien S, Chiou LK, Abbas PJ. Comparison of electrically evoked compound action potential thresholds and loudness estimates for the stimuli used to program the Advanced Bionics cochlear implant. J Am Acad Audiol 21: 16-27, 2010.
38. Jimenez Castellanos J. Thalamus of the cat in Horsley-Clarke coordinates. J Comp Neurol 91: 307-330, 1949.
39. Joksovic PM, Weiergraber M, Lee W, Struck H, Schneider T, Todorovic SM. Isoflurane-sensitive presynaptic R-type calcium channels contribute to inhibitory synaptic transmission in the rat thalamus. J Neurosci 29: 1434-1445, 2009.
40. Jones EG, Burton H. Cytoarchitecture and somatic sensory connectivity of thalamic nuclei other than the ventrobasal complex in the cat. J Comp Neurol 154: 395-432, 1974.
41. Kane A, Hutchison WD, Hodaie M, Lozano AM, Dostrovsky JO. Enhanced synchronization of thalamic theta band local field potentials in patients with essential tremor. Exp Neurol 217: 171-176, 2009.
42. Kemp JA, McKernan RM. NMDA receptor pathways as drug targets. Nat Neurosci 5, Suppl: 1039-1042, 2002.
43. Kent AR, Grill WM. Instrumentation to record evoked potentials for closedloop control of deep brain stimulation. Conf Proc IEEE Eng Med Biol Soc 2011: 6777-6780, 2011.
44. Kent AR, Grill WM. Recording evoked potentials during deep brain stimulation: development and validation of instrumentation to suppress the stimulus artefact. J Neural Eng 9: 036004, 2012.
45. Khodorov BL, Shishkova L, Peganov E, Revenko S. Inhibition of sodium currents in frog Ranvier node treated with local anesthetics. Role of slow sodium inactivation. Biochim Biophys Acta 433: 409-435, 1976.
46. Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, Koudsie A, Limousin PD, Benazzouz A, LeBas JF, Benabid AL, Pollak P. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 349: 1925-1934, 2003.
47. Krack P, Fraix V, Mendes A, Benabid AL, Pollak P. Postoperative management of subthalamic nucleus stimulation for Parkinson's disease. Mov Disord 17, Suppl 3: S188-S197, 2002.
48. Kultas-Ilinsky K, Fogarty JD, Hughes B, Ilinsky IA. Distribution and binding parameters of GABA and benzodiazepine receptors in the cat motor thalamus and adjacent nuclear groups. Brain Res 459: 1-16, 1988.
49. Kuncel AM, Cooper SE, Wolgamuth BR, Grill WM. Amplitude-and frequency-dependent changes in neuronal regularity parallel changes in tremor with thalamic deep brain stimulation. IEEE Trans Neural Syst Rehabil Eng 15: 190-197, 2007.
50. Kuncel AM, Grill WM. Selection of stimulus parameters for deep brain stimulation. Clin Neurophysiol 115: 2431-2441, 2004.
51. Lee JY, Jeon BS, Paek SH, Lim YH, Kim MR, Kim C. Reprogramming guided by the fused images of MRI and CT in subthalamic nucleus stimulation in Parkinson disease. Clin Neurol Neurosurg 112: 47-53, 2010.
52. Lempka SF, Johnson MD, Miocinovic S, Vitek JL, McIntyre CC. Currentcontrolled deep brain stimulation reduces in vivo voltage fluctuations observed during voltage-controlled stimulation. Clin Neurophysiol 121: 2128-2133, 2010.
53. Lenz FA, Seike M, Richardson RT, Lin YC, Baker FH, Khoja I, Jaeger CJ, Gracely RH. Thermal and pain sensations evoked by microstimulation in the area of human ventrocaudal nucleus. J Neurophysiol 70: 200-212, 1993.
54. Levy R, Lang AE, Dostrovsky JO, Pahapill P, Romas J, Saint-Cyr J, Hutchison WD, Lozano AM. Lidocaine and muscimol microinjections in subthalamic nucleus reverse Parkinsonian symptoms. Brain 124: 2105-2118, 2001.
55. Long SK, Smith DA, Siarey RJ, Evans RH. Effect of 6-cyano-2,3-dihydroxy-7-nitro-quinoxaline (CNQX) on dorsal root-, NMDA-, kainite-and quisqualate-mediated depolarization of rat motoneurones in vitro. Br J Pharmacol 100: 850-854, 1990.
56. Mallart A. Thalamic projection of muscle nerve afferents in the cat. J Physiol 194: 337-353, 1968.
57. Marceglia S, Rossi L, Foffani G, Bianchi A, Cerutti S, Priori A. Basal ganglia local field potentials: applications in the development of new deep brain stimulation devices for movement disorders. Expert Rev Med Devices 4: 605-614, 2007.
58. McConnell GC, Rees HD, Levey AI, Gutekunst CA, Gross RE, Bellamkonda RV. Implanted neural electrodes cause chronic, local inflammation that is correlated with local neurodegeneration. J Neural Eng 6: 056003, 2009.
59. McIntyre CC, Grill WM. Excitation of central nervous system neurons by nonuniform electric fields. Biophys J 76: 878-888, 1999.
60. McIntyre CC, Grill WM. Selective microstimulation of central nervous system neurons. Ann Biomed Eng 28: 219-233, 2000.
61. McIntyre CC, Grill WM, Sherman DL, Thakor NV. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J Neurophysiol 91: 1457-1469, 2004.
62. McIntyre CC, Richardson AG, Grill WM. Modeling the excitability of mammalian nerve fibers: influence of afterpotentials on the recovery cycle. J Neurophysiol 87: 995-1006, 2002.
63. McLaughlin M, Lu T, Dimitrijevic A, Zeng FG. Towards a closed-loop cochlear implant system: application of embedded monitoring of peripheral and central neural activity. IEEE Trans Neural Syst Rehabil Eng 20: 443-454, 2012.
64. Miller CA, Brown CJ, Abbas PJ, Chi SL. The clinical application of potentials evoked from the peripheral auditory system. Hear Res 242: 184-197, 2008.
65. Moffitt MA, McIntyre CC. Model-based analysis of cortical recording with silicon microelectrodes. Clin Neurophysiol 116: 2240-2250, 2005.
66. Moro E, Poon YY, Lozano AM, Saint-Cyr JA, Lang AE. Subthalamic nucleus stimulation: improvements in outcome with reprogramming. Arch Neurol 63: 1266-1272, 2006.
67. Noudoost B, Moore T. A reliable microinjectrode system for use in behaving monkeys. J Neurosci Methods 194: 218-223, 2011.
68. Okun MS, Tagliati M, Pourfar M, Fernandez HH, Rodriguez RL, Alterman RL, Foote KD. Management of referred deep brain stimulation failures: a retrospective analysis from 2 movement disorders centers. Arch Neurol 62: 1250-1255, 2005.
69. Ondo WG, Bronte-Stewart H. The North American survey of placement and adjustment strategies for deep brain stimulation. Stereotact Funct Neurosurg 83: 142-147, 2005.
70. Pahwa R, Lyons KE, Wilkinson SB, Simpson RK Jr, Ondo WG, Tarsy D, Norregaard T, Hubble JP, Smith DA, Hauser RA, Jankovic J. Longterm evaluation of deep brain stimulation of the thalamus. J Neurosurg 104: 506-512, 2006.
71. Posner LP, Burns P. Injectable anesthetic agents. In: Veterinary Pharmacology and Therapeutics, edited by Riviere JE, Papich MG. Ames, IA: Wiley-Blackwell, 2009, p. 265-300.
72. Rathnasingham R, Kipke DR, Bledsoe SC Jr, McLaren JD. Characterization of implantable microfabricated fluid delivery devices. IEEE Trans Biomed Eng 51: 138-145, 2004.
73. Ray NJ, Jenkinson N, Wang S, Holland P, Brittain JS, Joint C, Stein JF, 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 213: 108-113, 2008.
74. Rohatgi P, Langhals NB, Kipke DR, Patil PG. In vivo performance of a microelectrode neural probe with integrated drug delivery. Neurosurg Focus 27: E8, 2009.
75. Rosa M, Giannicola G, Servello D, Marceglia S, Pacchetti C, Porta M, Sassi M, Scelzo E, Barbieri S, Priori A. Subthalamic local field beta oscillations during ongoing deep brain stimulation in Parkinson's disease in hyperacute and chronic phases. Neurosignals 19: 151-162, 2011.
76. Rosin B, Slovik M, Mitelman R, Rivlin-Etzion M, Haber SN, Israel Z, Vaadia E, Bergman H. Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron 72: 370-384, 2011.
77. Santaniello S, Fiengo G, Glielmo L, Grill WM. Closed-loop control of deep brain stimulation: a simulation study. IEEE Trans Neural Syst Rehabil Eng 19: 15-24, 2011.
78. Sato F, Nakamura Y, Shinoda Y. Three-dimensional analysis of cerebellar terminals and their postsynaptic components in the ventral lateral nucleus of the cat thalamus. J Comp Neurol 371: 537-551, 1996.
79. Sherman SM. Interneurons and triadic circuitry of the thalamus. Trends Neurosci 27: 670-675, 2004.
80. Smirnov DA, Barnikol UB, Barnikol TT, Bezruchko BP, Hauptmann C, Buhrle C, Maarouf M, Sturm V, Freund HJ, Tass PA. The generation of parkinsonian tremor as revealed by directional coupling analysis. Europhys Lett 83: 1-6, 2008.
81. Snider RS, Niemer WT. A Stereotaxic Atlas of the Cat Brain. Chicago, IL: Univ. of Chicago Press, 1961.
82. Steriade M, Jones EG, McCormick DA. Thalamus. Oxford, UK: Elsevier Science, 1997.
83. Strichartz GR. The inhibition of sodium currents in myelinated nerve by quaternary derivatives of lidocaine. J Gen Physiol 62: 37-57, 1973.
84. Tamma F, Caputo E, Chiesa V, Egidi M, Locatelli M, Rampini P, Cinnante C, Pesenti A, Priori A. Anatomo-clinical correlation of intraoperative stimulation-induced side-effects during HF-DBS of the subthalamic nucleus. Neurol Sci 23, Suppl 2: S109-S110, 2002.
85. Tass P, Smirnov D, Karavaev A, Barnikol U, Barnikol T, Adamchic I, Hauptmann C, Pawelcyzk N, Maarouf M, Sturm V, Freund HJ, Bezruchko B. The causal relationship between subcortical local field potential oscillations and Parkinsonian resting tremor. J Neural Eng 7: 16009, 2010.
86. Tracey B, Williams M. Computationally efficient bioelectric field modeling and effects of frequency-dependent tissue capacitance. J Neural Eng 8: 036017, 2011.
87. Ulbricht W, Wagner HH. The influence of pH on equilibrium effects of tetrodotoxin on myelinated nerve fibres of Rana esculenta. J Physiol 252: 159-184, 1975.
88. Urbano F, Leznik E, Llinás R. Cortical activation patterns evoked by afferent axons stimuli at different frequencies: an in vitro voltage-sensitive dye imaging study. Thalamus Relat Syst 1: 371-378, 2002.
89. Wang LY, Kaczmarek LK. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394: 384-388, 1998.
90. Wang Q, Millard DC, Zheng HJ, Stanley GB. Voltage-sensitive dye imaging reveals improved topographic activation of cortex in response to manipulation of thalamic microstimulation parameters. J Neural Eng 9: 026008, 2012.
91. Weaver FM, Follett KA, Stern M, Luo P, Harris CL, Hur K, Marks WJ Jr, Rothlind J, Sagher O, Moy C, Pahwa R, Burchiel K, Hogarth P, Lai EC, Duda JE, Holloway K, Samii A, Horn S, Bronstein JM, Stoner G, Starr PA, Simpson R, Baltuch G, De Salles A, Huang GD, Reda DJ. Randomized trial of deep brain stimulation for Parkinson disease: thirtysix-month outcomes. Neurology 79: 55-65, 2012.
92. Wesseling JF, Lo DC. Limit on the role of activity in controlling the release-ready supply of synaptic vesicles. J Neurosci 22: 9708-9720, 2002.
93. Wu XS, Sun JY, Evers AS, Crowder M, Wu LG. Isoflurane inhibits transmitter release and the presynaptic action potential. Anesthesiology 100: 663-670, 2004.
94. Ying SW, Werner DF, Homanics GE, Harrison NL, Goldstein PA. Isoflurane modulates excitability in the mouse thalamus via GABA-dependent and GABA-independent mechanisms. Neuropharmacology 56: 438-447, 2009.
95. Yoshida F, Martinez-Torres I, Pogosyan A, Holl E, Petersen E, Chen CC, Foltynie T, Limousin P, Zrinzo LU, Hariz MI, Brown P. Value of subthalamic nucleus local field potentials recordings in predicting stimulation parameters for deep brain stimulation in Parkinson's disease. J Neurol Neurosurg Psychiatry 81: 885-889, 2010.
96. Yousif N, Bayford R, Liu X. The influence of reactivity of the electrode-brain interface on the crossing electric current in therapeutic deep brain stimulation. Neuroscience 156: 597-606, 2008.
97. Yousif N, Pavese N, Naushahi MJ, Nandi D, Bain PG. Reversing the polarity of bipolar stimulation in deep brain stimulation for essential tremor: a theoretical explanation for a useful clinical intervention. Neurocase (September 24, 2012). doi:10.1080/13554794.2012.713495.
98. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405, 2002.