Evolution of Deep Brain Stimulation: Human Electrometer and Smart Devices Supporting the Next Generation of Therapy
Correction(s) for this article
-
ERRATUM
- Volume 13Issue 4Neuromodulation: Technology at the Neural Interface
- pages: 322-322
- First Published online: October 6, 2010
Kendall H. Lee MD, PhD,
Charles D. Blaha PhD,
Paul A. Garris PhD,
Pedram Mohseni PhD,
April E. Horne MBA,
Kevin E. Bennet MBA,
Filippo Agnesi MS,
Jonathan M. Bledsoe MD,
Deranda B. Lester MS,
Chris Kimble MS,
Hoon-Ki Min MS,
Young-Bo Kim MD, PhD,
Zang-Hee Cho PhD,
Kendall H. Lee MD, PhD
Department of Neurosurgery and Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorCharles D. Blaha PhD
Department of Psychology, University of Memphis, Memphis, TN, USA;
Search for more papers by this authorPaul A. Garris PhD
Department of Biological Sciences, Illinois State University, Normal, IL, USA;
Search for more papers by this authorPedram Mohseni PhD
Electrical Engineering and Computer Science Department, Case Western Reserve University, Cleveland, OH, USA;
Search for more papers by this authorApril E. Horne MBA
Division of Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorKevin E. Bennet MBA
Division of Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorFilippo Agnesi MS
Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorJonathan M. Bledsoe MD
Department of Neurosurgery and Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorDeranda B. Lester MS
Department of Psychology, University of Memphis, Memphis, TN, USA;
Search for more papers by this authorChris Kimble MS
Division of Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorHoon-Ki Min MS
Neuroscience Research Institute, Gachon University of Medicine and Science, Incheon, South Korea
Search for more papers by this authorYoung-Bo Kim MD, PhD
Neuroscience Research Institute, Gachon University of Medicine and Science, Incheon, South Korea
Search for more papers by this authorZang-Hee Cho PhD
Neuroscience Research Institute, Gachon University of Medicine and Science, Incheon, South Korea
Search for more papers by this authorKendall H. Lee MD, PhD,
Charles D. Blaha PhD,
Paul A. Garris PhD,
Pedram Mohseni PhD,
April E. Horne MBA,
Kevin E. Bennet MBA,
Filippo Agnesi MS,
Jonathan M. Bledsoe MD,
Deranda B. Lester MS,
Chris Kimble MS,
Hoon-Ki Min MS,
Young-Bo Kim MD, PhD,
Zang-Hee Cho PhD,
Kendall H. Lee MD, PhD
Department of Neurosurgery and Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorCharles D. Blaha PhD
Department of Psychology, University of Memphis, Memphis, TN, USA;
Search for more papers by this authorPaul A. Garris PhD
Department of Biological Sciences, Illinois State University, Normal, IL, USA;
Search for more papers by this authorPedram Mohseni PhD
Electrical Engineering and Computer Science Department, Case Western Reserve University, Cleveland, OH, USA;
Search for more papers by this authorApril E. Horne MBA
Division of Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorKevin E. Bennet MBA
Division of Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorFilippo Agnesi MS
Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorJonathan M. Bledsoe MD
Department of Neurosurgery and Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorDeranda B. Lester MS
Department of Psychology, University of Memphis, Memphis, TN, USA;
Search for more papers by this authorChris Kimble MS
Division of Engineering, Mayo Clinic, Rochester, MN, USA;
Search for more papers by this authorHoon-Ki Min MS
Neuroscience Research Institute, Gachon University of Medicine and Science, Incheon, South Korea
Search for more papers by this authorYoung-Bo Kim MD, PhD
Neuroscience Research Institute, Gachon University of Medicine and Science, Incheon, South Korea
Search for more papers by this authorZang-Hee Cho PhD
Neuroscience Research Institute, Gachon University of Medicine and Science, Incheon, South Korea
Search for more papers by this authorAddress correspondence and reprint requests to: Kendall Lee, MD, PhD, Departments of Neurosurgery and Physiology and Biomedical Engineering, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA. Email: [email protected]
ABSTRACT
Deep brain stimulation (DBS) provides therapeutic benefit for several neuropathologies, including Parkinson disease (PD), epilepsy, chronic pain, and depression. Despite well-established clinical efficacy, the mechanism of DBS remains poorly understood. In this review, we begin by summarizing the current understanding of the DBS mechanism. Using this knowledge as a framework, we then explore a specific hypothesis regarding DBS of the subthalamic nucleus (STN) for the treatment of PD. This hypothesis states that therapeutic benefit is provided, at least in part, by activation of surviving nigrostriatal dopaminergic neurons, subsequent striatal dopamine release, and resumption of striatal target cell control by dopamine. While highly controversial, we present preliminary data that are consistent with specific predications testing this hypothesis. We additionally propose that developing new technologies (e.g., human electrometer and closed-loop smart devices) for monitoring dopaminergic neurotransmission during STN DBS will further advance this treatment approach.
References
- 1 Benabid AL. Deep brain stimulation for Parkinson's disease. Curr Opin Neurobiol 2003; 13: 696–706.
- 2 Deuschl G, Schade-Brittinger C, Krack P et al. A randomized trial of deep-brain stimulation for Parkinson's disease. N Engl J Med 2006; 355: 896–908.
- 3 Benabid AL, Pollak P, Seigneuret E, Hoffmann D, Gay E, Perret J. Chronic VIM thalamic stimulation in Parkinson's disease, essential tremor and extra-pyramidal dyskinesias. Acta Neurochir Suppl (Wien) 1993; 58: 39–44.
- 4 Greene P. Deep-brain stimulation for generalized dystonia. N Engl J Med 2005; 352: 498–500.
- 5 Hodaie M, Wennberg RA, Dostrovsky JO, Lozano AM. Chronic anterior thalamus stimulation for intractable epilepsy. Epilepsia 2002; 43: 603–608.
- 6 Boon P, De Vonck KHV, Van Dycke A et al. Deep brain stimulation in patients with refractory temporal lobe epilepsy. Epilepsia 2007; 48: 1551–1560.
- 7 Vonck K, Boon P, Van Roost D. Anatomical and physiological basis and mechanism of action of neurostimulation for epilepsy. Acta Neurochir Suppl 2007; 97: 321–328.
- 8 Bittar RG, Kar-Purkayastha I, Owen SL et al. Deep brain stimulation for pain relief: a meta-analysis. J Clin Neurosci 2005; 12: 515–519.
- 9 Rasche D, Rinaldi PC, Young RF, Tronnier VM. Deep brain stimulation for the treatment of various chronic pain syndromes. Neurosurg Focus 2006; 21: E8.
- 10 Maciunas RJ, Maddux BN, Riley DE et al. Prospective randomized double-blind trial of bilateral thalamic deep brain stimulation in adults with Tourette syndrome. J Neurosurg 2007; 107: 1004–1014.
- 11 Greenberg BD, Malone DA, Friehs GM et al. Three-year outcomes in deep brain stimulation for highly resistant obsessive-compulsive disorder. Neuropsychopharmacology 2006; 31: 2384–2393.
- 12 Lipsman N, Neimat JS, Lozano AM. Deep brain stimulation for treatment-refractory obsessive-compulsive disorder: the search for a valid target. Neurosurgery 2007; 61: 1–11.
- 13 Mayberg HS, Lozano AM, Voon V et al. Deep brain stimulation for treatment-resistant depression. Neuron 2005; 45: 651–660.
- 14 Hardesty DE, Sackeim HA. Deep brain stimulation in movement and psychiatric disorders. Biol Psychiatry 2007; 61: 831–835.
- 15 Schlaepfer TE, Cohen MX, Frick C et al. Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 2008; 33: 368–377.
- 16
McIntyre CC,
Butson CR,
Maks CB,
Noecker AM.
Optimizing deep brain stimulation parameter selection with detailed models of the electrode–tissue interface.
Conf Proc IEEE Eng Med Biol Soc
2006; 115: 893–895.
10.1109/IEMBS.2006.260844 Google Scholar
- 17 Lee KH, Blaha CD, Bledsoe JM. Mechanisms of action of deep brain stimulation: a review. In: E Krames, H Peckham, A Rezai, eds. A Textbook of Neuromodulation. Amsterdam, The Netherlands: Elsevier, 2008: 1–25.
- 18 Benabid AL, 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.
- 19 Bergman H, Wichmann T, DeLong MR. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 1990; 249: 1436–1438.
- 20 Benazzouz A, Piallat B, Pollak P, Benabid AL. Responses of substantia nigra pars reticulata and globus pallidus complex to high frequency stimulation of the subthalamic nucleus in rats: electrophysiological data. Neurosci Lett 1995; 189: 77–80.
- 21 Patel NK, Heywood P, O'Sullivan K, McCarter R, Love S, Gill SS. Unilateral subthalamotomy in the treatment of Parkinson's disease. Brain 2003; 126: 1136–1145.
- 22 Benazzouz A, Hallett M. Mechanism of action of deep brain stimulation. Neurology 2000; 55: S13–S16.
- 23 McIntyre CC, Thakor NV. Uncovering the mechanisms of deep brain stimulation for Parkinson's disease through functional imaging, neural recording, and neural modeling. Crit Rev Biomed Eng 2002; 30: 249–281.
- 24 Lozano AM, Eltahawy H. How does DBS work? Suppl Clin Neurophysiol 2004; 57: 733–736.
- 25 McIntyre CC, Savasta M, Kerkerian-Le Goff L, Vitek JL. Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin Neurophysiol 2004; 115: 1239–1248.
- 26 Perlmutter JS, Mink JW. Deep brain stimulation. Annu Rev Neurosci 2006; 29: 229–257.
- 27 Uc EY, Follett KA. Deep brain stimulation in movement disorders. Semin Neurol 2007; 27: 170–182.
- 28 Beurrier C, Bioulac B, Audin J, Hammond C. High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J Neurophysiol 2001; 85: 1351–1356.
- 29 Magarinos-Ascone C, Pazo JH, Macadar O, Buno W. High-frequency stimulation of the subthalamic nucleus silences subthalamic neurons: a possible cellular mechanism in Parkinson's disease. Neuroscience 2002; 115: 1109–1117.
- 30 Lee KH, Blaha CD, Harris BT et al. 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.
- 31 McIntyre CC, Gril WM, Sherman DL, Thakor NV. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J Neurophysiol 2004; 91: 1457–1469.
- 32 McIntyre CC, Savasta M, Walter BL, Vitek JL. How does deep brain stimulation work? Present understanding and future questions. J Clin Neurophysiol 2004; 21: 40–50.
- 33 Limousin P, Krack P, Pollak P et al. Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 1998; 339: 1105–1111.
- 34 Volkmann J. Deep brain stimulation for the treatment of Parkinson's disease. J Clin Neurophysiol 2004; 21: 6–17.
- 35 Moro E, Scerrati M, Romito LM, Roselli R, Tonali P, Albanese A. Chronic subthalamic nucleus stimulation reduces medication requirements in Parkinson's disease. Neurology 1999; 53: 85–90.
- 36 Molinuevo JL, Valldeoriola F, Tolosa E et al. Levodopa withdrawal after bilateral subthalamic nucleus stimulation in advanced Parkinson disease. Arch Neurol 2000; 57: 983–988.
- 37 Agid Y. Parkinson's disease: pathophysiology. Lancet 1991; 337: 1321–1324.
- 38 Lang AE, Lozano AM. Parkinson's disease. First of two parts. N Engl J Med 1998; 339: 1044–1153.
- 39 Lang AE, Lozano AM. Parkinson's disease. Second of two parts. N Engl J Med 1998; 339: 1130–1143.
- 40 Gerlach M, van den Buuse M, Blaha CD, Bremen D, Riederer P. Entacapone increases and prolongs the central effects of L-DOPA in the 6-hyroxydopamine-lesioned rat. Naunyn-Schmied Arch Pharmac 2004; 370: 388–394.
- 41 Breit S, Schulz JB, Benabid AL. Deep brain stimulation. Cell Tissue Res 2004; 318: 275–288.
- 42 Kern DS, Kumar R. Deep brain stimulation. Neurologist 2007; 13: 237–252.
- 43 Frank MJ, Samanta J, Moustafa AA, Sherman SJ. Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science 2007; 318: 1309–1312.
- 44 Bruet N, Windels F, Bertrand A, Feuerstein C, Poupard A, Savasta M. High frequency stimulation of the subthalamic nucleus increases the extracellular contents of striatal dopamine in normal and partially dopaminergic denervated rats. J Neuropathol Exp Neurol 2001; 60: 15–24.
- 45 Paul G, Reum T, Meissner W et al. High frequency stimulation of the subthalamic nucleus influences striatal dopaminergic metabolism in the naive rat. Neuroreport 2000; 11: 441–444.
- 46 Meissner W, Reum T, Paul G et al. Striatal dopaminergic metabolism is increased by deep brain stimulation of the subthalamic nucleus in 6-hydroxydopamine lesioned rats. Neurosci Lett 2001; 303: 165–168.
- 47 Meissner W, Harnack D, Paul G et al. Deep brain stimulation of subthalamic neurons increases striatal dopamine metabolism and induces contralateral circling in freely moving 6-hydroxydopamine-lesioned rats. Neurosci Lett 2002; 328: 105–108.
- 48 Abosch A, Kapur S, Lang AE et al. Stimulation of the subthalamic nucleus in Parkinson's disease does not produce striatal dopamine release. Neurosurgery 2003; 53: 1095–1102.
- 49 Hilker R, Voges J, Ghaemi M et al. Deep brain stimulation of the subthalamic nucleus does not increase the striatal dopamine concentration in parkinsonian humans. Mov Disord 2003; 18: 41–48.
- 50 Thobois S, Fraix V, Savasta M et al. Chronic subthalamic nucleus stimulation and striatal D2 dopamine receptors in Parkinson's disease: a [11C]-raclopride PET study. J Neurol 2003; 250: 219–223.
- 51 Volkow ND, Fowler JS, Wang GJ et al. Reproducibility of repeated measures of carbon-11-raclopride binding in the human brain. J Nucl Med 1993; 34: 609–613.
- 52 Laruelle M, Slifstein M, Huang Y. Positron emission tomography: imaging and quantification of neurotransporter availability. Methods 2002; 27: 287–299.
- 53 Albin RL, Young AB, Penney JB. The functional anatomy of basal ganglia disorders. Trends Neurosci 1989; 12: 366–375.
- 54 Graybiel AM. Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci 1990; 13: 244–254.
- 55 Overton PG, Clark D. Burst firing in midbrain dopaminergic neurons. Brain Res Rev 1997; 25: 312–334.
- 56 Kitai ST, Shepard PD, Callaway JC, Scroggs R. Afferent modulation of dopamine neuron firing patterns. Curr Opin Neurobiol 1999; 9: 690–697.
- 57 Woolf NJ. Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 1991; 37: 475–524.
- 58
Garzón M,
Vaughan RA,
Uhl GR,
Kuhar MJ,
Pickel VM.
Cholinergic axon terminals in the ventral tegmental area target a subpopulation of neurons expressing low levels of the dopamine transporter.
J Comp Neurol
1999; 410: 197–210.
10.1002/(SICI)1096-9861(19990726)410:2<197::AID-CNE3>3.0.CO;2-D CAS PubMed Web of Science® Google Scholar
- 59 Grillner P, Mercuri NB. Intrinsic membrane properties and synaptic inputs regulating the firing activity of the dopamine neurons. Behav Brain Res 2002; 130: 149–169.
- 60 McGinty JF. Co-localization of GABA with other neuroactive substances in the basal ganglia. Prog Brain Res 2007; 160: 273–284.
- 61 Meltzer LT, Christoffersen CL, Serpa KA. Modulation of dopamine neuronal activity by glutamate receptor subtypes. Neurosci Biobehav Rev 1997; 21: 511–518.
- 62 Blaha CD, Winn P. Modulation of dopamine efflux in the striatum following cholinergic stimulation of the substantia nigra in intact and pedunculopontine tegmental nucleus-lesioned rats. J Neurosci 1993; 13: 1035–1044.
- 63 Blaha CD, Allen LF, Das S et al. Modulation of dopamine efflux in the nucleus accumbens after cholinergic stimulation of the ventral tegmental area in intact, pedunculopontine tegmental nucleus-lesioned, and laterodorsal tegmental nucleus-lesioned rats. J Neurosci 1996; 16: 714–722.
- 64 Forster GL, Blaha CD. Pedunculopontine tegmental stimulation evokes striatal dopamine efflux by activation of acetylcholine and glutamate receptors in the midbrain and pons of the rat. Eur J Neurosci 2003; 17: 751–762.
- 65 Paladini CA, Celada P, Tepper JM. Striatal, pallidal, and pars reticulata evoked inhibition of nigrostriatal dopaminergic neurons is mediated by GABAA receptors in vivo. Neuroscience 1999; 89: 799–812.
- 66 Celada P, Paladini CA, Tepper JM. GABAergic control of nigra dopamine neurons: role of globus pallidus and nigra reticulata. Neuroscience 1999; 89: 813–825.
- 67 Iribe Y, Moore K, Pang KC, Tepper JM. Subthalamic stimulation-induced synaptic responses in substantia nigra pars compacta dopaminergic neurons in vitro. J Neurophys 1999; 82: 925–933.
- 68 Shen KZ, Zhu ZT, Munhall A, Johnson SW. Synaptic plasticity in rat subthalamic nucleus induced by high-frequency stimulation. Synapse 2003; 50: 314–319.
- 69 Lee KH, Chang SY, Roberts DW, Kim U. Neurotransmitter release from high-frequency stimulation of the subthalamic nucleus. J Neurosurg 2004; 101: 511–517.
- 70 Lee KH, Kristic K, van Hoff R et al. High frequency stimulation of the subthalamic nucleus increases glutamate in the subthalamic nucleus of rats as demonstrated by in vivo enzyme-linked glutamate sensor. Brain Res 2007; 1162: 121–129.
- 71 Lee KH, Hitti FL, Shalinsky MH, Kim U, Leiter JC, Roberts DW. Abolition of spindle oscillations and 3-Hz absence seizurelike activity in the thalamus by using high-frequency stimulation: potential mechanism of action. J Neurosurg 2005; 103: 538–545.
- 72 Vernadakis A, Lee K, Kentroti S, Brodie C. Role of astrocytes in aging. late passage primary mouse brain astrocytes and C-6 glial cells as models. Prog Brain Res 1992; 94: 391–409.
- 73 Lee KH, Hitti FL, Tawfik VL et al. High frequency stimulation abolishes network oscillations by astrocytic glutamate release. Program no. 898.2. Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2005.
- 74 Benazzouz A, Gao D, Ni Z, Benabid AL. High frequency stimulation of the STN influences the activity of dopamine neurons in the rat. Neuroreport 2000; 11: 1593–1596.
- 75 Benazzouz A, Piallat B, Ni Z, Koudsie G, Pollak A, Benabid AL. Implication of the subthalamic nucleus in the pathophysiology and pathogenesis of Parkinson's disease. Cell Transplant 2000; 9: 215–221.
- 76 Hammond C, Deniau JM, Rizk A, Feger J. Electrophysiological demonstration of an excitatory subthalamonigral pathway in the rat. Brain Res 1978; 151: 235–244.
- 77 Smith ID, Grace AA. Role of the subthalamic nucleus in the regulation of nigral dopamine neuron activity. Synapse 1992; 12: 287–303.
- 78 Garris PA, Kilpatrick M, Bunin MA, Michael D, Walker QD, Wightman RM. Dissociation of dopamine release in the nucleus accumbens from intracranial self-stimulation. Nature 1999; 398: 67–69.
- 79 Bergstrom BP, Garris PA. Utility of a tripolar stimulating electrode for eliciting dopamine release in the rat striatum. J Neurosci Methods 1999; 87: 201–208.
- 80 Bergstrom BP, Garris PA. ‘Passive stabilization’ of striatal extracellular dopamine across the lesion spectrum encompassing the presymptomatic phase of Parkinson's disease: a voltammetric study in the 6-OHDA-lesioned rat. J Neurochem 2003; 87: 1224–1236.
- 81 Clapp-Lilly KL, Roberts RC, Duffy LK, Irons KP, Hu Y, Drew KL. An ultrastructural analysis of tissue surrounding a microdialysis probe. J Neurosci Methods 1999; 90: 129–142.
- 82 Tang A, Bungay PM, Gonzales RA. Characterization of probe and tissue factors that influence interpretation of quantitative microdialysis experiments for dopamine. J Neurosci Methods 2003; 126: 1–11.
- 83 Borland LM, Shi G, Yang H, Michael AC. Voltammetric study of extracellular dopamine near microdialysis probes acutely implanted in the striatum of the anesthetized rat. J Neurosci Methods 2005; 146: 149–158.
- 84 Morelli M, Carboni E, Cozzolino A, Tanda GL, Pinna A, Di Chiara G. Combined microdialysis and Fos immunohistochemistry for the estimation of dopamine neurotransmission in the rat caudate-putamen. J Neurochem 1992; 59: 1158–1160.
- 85 Di Chiara G, Carboni E, Morelli M et al. Stimulation of dopamine transmission in the dorsal caudate nucleus by pargyline as demonstrated by dopamine and acetylcholine microdialysis and Fos immunohistochemistry. Neuroscience 1993; 55: 451–456.
- 86 Blaha CD, Phillips AG. A critical assessment of electrochemical procedures applied to the measurement of dopamine and its metabolites during drug-induced and species-typical behaviours. Behav Pharmacol 1996; 7: 675–708.
- 87 Blaha CD, Coury A, Phillips AG. Does monoamine oxidase inhibition by pargyline increase extracellular dopamine concentrations in the striatum? Neuroscience 1996; 75: 543–550.
- 88 Peters JL, Miner LH, Michael AC, Sesack SR. Ultrastructure at carbon fiber microelectrode implantation sites after acute voltammetric measurements in the striatum of anesthetized rats. J Neurosci Methods 2004; 137: 9–23.
- 89 Cheer JF, Heien ML, Garris PA, Carelli RM, Wightman RM. Simultaneous electrochemical and single-unit recordings in the nucleus accumbens reveal GABA-mediated responses: implications for intracranial self-stimulation. Proc Natl Acad Sci USA 2005; 102: 19150–19155.
- 90 Zigmond MJ, Abercrombie ED, Berger TW, Grace AA, Stricker EM. Compensations after lesions of central dopaminergic neurons: some clinical and basic implications. Trends Neurosci 1990; 13: 290–296.
- 91 Hornykiewicz O, Kish SJ. Biochemical pathophysiology of Parkinson's disease. Adv Neurol 1987; 45: 19–34.
- 92 Saint-Cyr JA, Hoque T, Pereira LC et al. Localization of clinically effective stimulating electrodes in the human subthalamic nucleus on magnetic resonance imaging. J Neurosurg 2002; 97: 1152–1166.
- 93 Voges J, Volkmann J, Allert N et al. Bilateral high-frequency stimulation in the subthalamic nucleus for the treatment of Parkinson disease: correlation of therapeutic effect with anatomical electrode position. J Neurosurg 2002; 96: 269–279.
- 94 Herzog J, Fietzek U, Hamel W et al. Most effective stimulation site in subthalamic deep brain stimulation for Parkinson's disease. Mov Disord 2004; 19: 1050–1054.
- 95 Chang J-Y, Shi L-H, Luo F, Zhang W-M, Woodward DJ. Studies of the neural mechanisms of deep brain stimulation in rodent models of Parkinson's disease. Neurosci Biobehav Rev 2007; 31: 643–657.
- 96 Blaha CD, Phillips AG. Application of in vivo electrochemistry to the measurement of changes in dopamine release during intracranial self-stimulation. J Neurosci Methods 1990; 34: 125–133.
- 97 Kilpatrick MR, Rooney MB, Michael DJ, Wightman RM. Extracellular dopamine dynamics in rat caudate-putamen during experimenter-delivered and intracranial self-stimulation. Neuroscience 2000; 96: 697–706.
- 98 Yavich L, Tiihonen J. In vivo voltammetry with removable carbon fibre electrodes in freely-moving mice: dopamine release during intracranial self-stimulation. J Neurosci Methods 2000; 104: 55–63.
- 99 Cheer JF, Wassum KM, Heien ML, Phillips PE, Wightman RM. Cannabinoids enhance subsecond dopamine release in the nucleus accumbens of awake rats. J Neurosci 2004; 24: 4393–4400.
- 100 Carelli RM, Wightman RM. Functional microcircuitry in the accumbens underlying drug addiction: insights from real-time signaling during behavior. Curr Opin Neurobiol 2004; 14: 763–768.
- 101 Schultz W. Behavioral dopamine signals. Trends Neurosci 2007; 30: 203–210.
- 102 Schultz W. Multiple dopamine functions at different time courses. Annu Rev Neurosci 2007; 30: 259–288.
- 103 Garris PA, Ensman R, Poehlman J et al. Wireless transmission of fast-scan cyclic voltammetry at a carbon-fiber microelectrode: proof of principle. J Neurosci Methods 2004; 140: 103–115.
- 104
Garris PA,
Greco PG,
Sandberg SG et al. In vivo voltammetry with telemetry. In: AC Michael,
LM Borland, eds. Electrochemical Methods for Neuroscience. Boca Raton, FL: CRC Press, 2006: 233–259.
10.1201/9781420005868.ch12 Google Scholar
- 105 Agnesi F, Tye S, Blaha C, Garris P, Goerss S, Sieck G, Stead M, Lee KH. Complex electrophysiological correlates to deep brain stimulation in patients with Parkinson's disease, dystonia, and essential tremor. Abstract. Washington, DC. Society for Neuroscience, 2008.
- 106 Roham M, Daberkow DP, Ramsson ES et al. A wireless IC for wide-range neurochemical monitoring using amperometry and fast-scan cyclic voltammetry. IEEE Trans Biomed Circuits Systems 2008; 2: 3–9.
