The T-type calcium channel as a new therapeutic target for Parkinson's disease

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 4, 2014, Pages 747-755

  Yang, Ya Chin ^a   Tai, Chun Hwei ^b   Pan, Ming Kai ^b,c   Kuo, Chung Chin ^b,c  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Basal ganglia; Burst discharges; Deep brain stimulation; Neural rhythms; Subthalamus

Indexed keywords

CALCIUM CHANNEL T TYPE; DOPAMINE; DOPAMINE RECEPTOR; ZONISAMIDE;

BASAL GANGLION; BRADYKINESIA; BRAIN DEPTH STIMULATION; CELL MEMBRANE; CLINICAL EFFECTIVENESS; DOPAMINERGIC NERVE CELL; ELECTRIC ACTIVITY; ELECTRIC CURRENT; EXTRACELLULAR SPACE; GLOBUS PALLIDUS; HUMAN; LIPID BILAYER; LOCOMOTION; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MEMBRANE STEADY POTENTIAL; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PLASMA PROTEIN BINDING; POSITIVE FEEDBACK; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RIGIDITY; SPIKE; SUBTHALAMIC NUCLEUS; TREMOR; ACTION POTENTIAL; ANIMAL; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; TRENDS;

ACTION POTENTIALS; ANIMALS; CALCIUM CHANNELS, T-TYPE; DEEP BRAIN STIMULATION; DOPAMINE; HUMANS; NEURONS; PARKINSON DISEASE; SUBTHALAMIC NUCLEUS;

EID: 84896548109     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1466-6     Document Type: Review

References (84)

1. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-375 (Pubitemid 19238787)
2. Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:266-271 (Pubitemid 20193456)
3. Alvarez L, Macias R, Pavón N, López G, Rodríguez- Oroz MC, Rodríguez R, Alvarez M, Pedroso I, Teijeiro J, Fernández R, Casabona E, Salazar S, Maragoto C, Carballo M, García I, Guridi J, Juncos JL, DeLong MR, Obeso JA (2009) Therapeutic efficacy of unilateral subthalamotomy in Parkinson's disease: results in 89 patients followed for up to 36 months. J Neurol Neurosurg Psychiatry 80:979-985
4. Amtage F, Henschel K, Schelter B, Vesper J, Timmer J, Lucking CH, Hellwig B (2008) Tremor-correlated neuronal activity in the subthalamic nucleus of Parkinsonian patients. Neurosci Lett 442:195-199
5. Bal T, von Krosigk M, McCormick DA (1995) Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro. J Physiol 483:641-663
6. Benabid AL, Chabardes S, Mitrofanis J, Pollak P (2009) Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's disease. Lancet Neurol 8(1):67-81
7. Benabid AL, Pollak P, Gross C, Hoffmann D, Benazzouz A, Gao DM, Laurent A, Gentil M, Perret J (1994) Acute and long-term effects of subthalamic nucleus stimulation in Parkinson's disease. Stereotact Funct Neurosurg 62(1-4):76-84
8. Benazzouz A, Breit S, Koudsie A, Pollak P, Krack P, Benabid AL (2002) Intraoperative microrecordings of the subthalamic nucleus in Parkinson's disease. Mov Disord 17(Suppl 3):S145-S149 (Pubitemid 36040918)
9. Bergman H, Wichmann T, Karmon B, DeLong MR (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72(2):507-520 (Pubitemid 24273560)
10. Beurrier C, Bioulac B, Hammond C (2000) Slowly inactivating sodium current (I(NaP)) underlies single spike activity in rat subthalamic neurons. J Neurophysiol 83(4):1951-1957 (Pubitemid 30198651)
11. Beurrier C, Congar P, Bioulac B, Hammond C (1999) Subthalamic nucleus neurons switch from single-spike activity to burst-firing mode. J Neurosci 19(2):599-609 (Pubitemid 29036011)
12. Bevan MD, Wilson CJ (1999) Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J Neurosci 19(17):7617-7628 (Pubitemid 29404617)
13. Cain SM, Snutch TP (2013) T-type calcium channels in burst-firing, network synchrony, and epilepsy. Biochim Biophys Acta 1828:1572-1578
14. Cragg S, Baufreton J, Xue Y, Bolam J, Bevan MD (2004) Synaptic release of dopamine in the subthalamic nucleus. Eur J Neurosci 20(7):1788-1802 (Pubitemid 39471572)
15. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281-285
16. DeLong MR, Wichmann T (2007) Circuits and circuit disorders of the basal ganglia. Arch Neurol 64:20-24 (Pubitemid 46072419)
17. Do MT, Bean BP (2003) Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39(1):109-120 (Pubitemid 36830952)
18. Elble RJ (1996) Central mechanisms of tremor. J Clin Neurophysiol 13:133-144
19. Elble RJ (2000) Origins of tremor. Lancet 355:1113-1114
20. Enomoto A, Han JM, Hsiao CF, Wu N, Chandler SH (2006) Participation of sodium currents in burst generation and control of membrane excitability in mesencephalic trigeminal neurons. J Neurosci 26(13):3412-3422
21. Filion M, Tremblay L (1991) Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res 547:142-151
22. Francois C, Savy C, Jan C, Tande D, Hirsch EC, Yelnik J (2000) Dopaminergic innervations of the subthalamic nucleus in the normal state, in MPTP treated monkeys, and in Parkinson's disease patients. J Comp Neurol 425:121-129
23. Georgopoulos AP, DeLong MR, Crutcher MD (1983) Relations between parameters of step-tracking movements and single cell discharge in the globus pallidus and subthalamic nucleus of the behaving monkey. J Neurosci 3(8):1586-1598 (Pubitemid 13045295)
24. Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN, Monsma FJ Jr, Sibley DR (1990) D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250:1429-1432 (Pubitemid 120031867)
25. Govindaiah G, Cox CL (2005) Excitatory actions of dopamine via D1-like receptors in the rat lateral geniculate nucleus. J Neurophysiol 94:3708-3718 (Pubitemid 41691738)
26. Guridi J, Herrero MT, Luquin MR, Guillen J, Ruberg M, Laguna J, Vila M, Javoy-Agid F, Agid Y, Hirsch E, Obeso JA (1996) Subthalamotomy in parkinsonian monkeys. Behavioural and biochemical analysis. Brain 119(5):1717-1727 (Pubitemid 26376797)
27. Hamani C, Neimat JS, Lozano AM (2007) Deep brain stimulation and chemical neuromodulation: current use and perspectives for the future. Acta Neurochir 97(2):127-133
28. Hassani OK, Féger J (1999) Effects of intrasubthalamic injection of dopamine receptor agonists on subthalamic neurons in normal and 6-hydroxydopamine-lesioned rats: an electrophysiological and c-Fos study. Neuroscience 92(2):533-543
29. Hellwig B, Haussler S, Lauk M, Guschlbauer B, Koster B, Kristeva-Feige R, Timmer J, Lücking CH (2000) Tremor-correlated cortical activity detected by electroencephalography. Clin Neurophysiol 111:806-809 (Pubitemid 30236425)
30. Hikosaka O, Takikawa Y, Kawagoe R (2000) Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80:953-978 (Pubitemid 30452008)
31. Holder JL Jr, Wilfong AA (2011) Zonisamide in the treatment of epilepsy. Expert Opin Pharmacother 12(16):2573-2581
32. Hollerman JR, Grace AA (1992) Subthalamic nucleus cell firing in the 6-OHDA-treated rat: basal activity and response to haloperidol. Brain Res 590:291-299
33. Hurtado JM, Gray CM, Tamas LB, Sigvardt KA (1999) Dynamics of tremor-related oscillations in the human globus pallidus: a single case study. Proc Natl Acad Sci U S A 96:1674-1679 (Pubitemid 29098510)
34. Hutchison WD, Allan RJ, Opitz H, Levy R, Dostrovsky JO, Lang AE, Lozano AM (1998) Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson's disease. Ann Neurol 44:622-628 (Pubitemid 28477849)
35. Jahnsen H, Llinas R (1984) Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol 349:205-226 (Pubitemid 14060329)
36. Jahnsen H, Llinas R (1984) Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol 349:227-247 (Pubitemid 14060330)
37. Kito M, Maehara M, Watanabe K (1996) Mechanisms of T-type calcium channel blockade by zonisamide. Seizure 5:115-119 (Pubitemid 26232348)
38. Krack P, Limousin P, Benabid AL, Pollak P (1997) Chronic stimulation of subthalamic nucleus improves levodopa-induced dyskinesias in Parkinson's disease. Lancet 350:1676 (Pubitemid 28036831)
39. Kreiss DS, Mastropietro CW, Rawji SS, Walters JR (1997) The response of subthalamic nucleus neurons to dopamine receptor stimulation in a rodent model of Parkinson's disease. J Neurosci 17(17):6807-6819
40. Lenz FA, Kwan HC, Martin RL, Tasker RR, Dostrovsky JO, Lenz YE (1994) Single unit analysis of the human ventral thalamic nuclear group. Tremor-related activity in functionally identified cells. Brain 117(3):531-543
41. Leppik IE (1999) Zonisamide. Epilepsia 40(Suppl 5):S23-S29
42. Limousin P, Krack P, Pollak P, Benazzouz A, Ardouin C, Hoffmann D, Benabid AL (1998) Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 339:1105-1111 (Pubitemid 28465758)
43. Llinas R, Jahnsen H (1982) Electrophysiology of mammalian thalamic neurones in vitro. Nature 297:406-408
44. Limousin P, Pollak P, Benazzouz A, Hoffmann D, Broussolle E, Perret JE, Benabid AL (1995) Bilateral subthalamic nucleus stimulation for severe Parkinson's disease. Mov Disord 10(5):672-674
45. Limousin P, Pollak P, Benazzouz A, Hoffmann D, Le Bas JF, Broussolle E, Perret JE, Benabid AL (1995) Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 345(8942):91-95
46. Llinas R, Yarom Y (1981) Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. J Physiol 315:549-567 (Pubitemid 11072016)
47. Mallet N, Ballion B, Le Moine C, Gonon F (2006) Cortical inputs and GABAinterneurons imbalance projection neurons in the striatum of parkinsonian rats. J Neurosci 26(14):3875-3884
48. Marchand R (1987) Histogenesis of the subthalamic nucleus. Neuroscience 21:183-195
49. Matar N, Jin W, Wrubel H, Hescheler J, Schneider T, Weiergräber M (2009) Zonisamide block of cloned human T-type voltage-gated calcium channels. Epilepsy Res 83:224-234
50. McCormick DA, Bal T (1994) Sensory gating mechanisms of the thalamus. Curr Opin Neurobiol 4:550-556 (Pubitemid 24258915)
51. McCormick DA, Bal T (1997) Sleep and arousal: thalamocortical mechanisms. Annu Rev Neurosci 20:185-215 (Pubitemid 27106380)
52. Mimaki T (1998) Clinical pharmacology and therapeutic drug monitoring of zonisamide. Ther Drug Monit 20:593-597
53. Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381-425
54. Mink JW (2003) The basal ganglia and involuntary movements: impaired inhibition of competing motor patterns. Arch Neurol 60(10):1365-1368
55. Miwa H (2007) Zonisamide for the treatment of Parkinson's disease. Expert Rev Neurother 7(9):1077-1083
56. Murata M, Hasegawa K, Kanazawa I, Japan Zonisamide on PD Study Group (2007) Zonisamide improves motor function in Parkinson disease: a randomized, double-blind study. Neurology 68:45-50 (Pubitemid 46058551)
57. Murata M, Horiuchi E, Kanazawa I (2001) Zonisamide has beneficial effects on Parkinson's disease patients. Neurosci Res 41:397-399 (Pubitemid 33733759)
58. Nakanishi H, Kita H, Kitai ST (1987) Electrical membrane properties of rat subthalamic neurons in an in vitro slice preparation. Brain Res 437(1):35-44 (Pubitemid 18029686)
59. Nambu A (2005) A new approach to understand the pathophysiology of Parkinson's disease. J Neurol 252(Suppl 4):IV1-IV4
60. Nambu A, Tokuno H, Takada M (2002) Functional significance of the cortico-subthalamo-pallidal 'hyperdirect' pathway. Neurosci Res 43(2):111-117 (Pubitemid 34627041)
61. Ni ZG, Bouali-Benazzouz R, Gao DM, Benabid AL, Benazzouz A (2001) Time-course of changes in firing rates and firing patterns of subthalamic nucleus neuronal activity after 6-OHDA-induced dopamine depletion in rats. Brain Res 899:142-147 (Pubitemid 32324155)
62. Nicola SM (2007) The nucleus accumbens as part of a basal ganglia action selection circuit. Psychopharmacology (Berlin) 191:521-550
63. Obeso JA, Rodriguez-Oroz MC, Rodriguez M, Lanciego JL, Artieda J, Gonzalo N, Olanow CW (2000) Pathophysiology of the basal ganglia in Parkinson's disease. Trends Neurosci 23:S8-S19
64. Oommen KJ, Mathews S (1999) Zonisamide: a new antiepileptic drug. Clin Neuropharmacol 22:192-200 (Pubitemid 30004134)
65. Packard MG, Knowlton BJ (2002) Learning and memory functions of the basal ganglia. Annu Rev Neurosci 25:563-593 (Pubitemid 34748029)
66. Perez-Reyes E (2003) Molecular physiology of low-voltage-activated T-type calcium channels. Physiol Rev 83:117-161
67. Plenz D, Kital ST (1999) A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400(6745): 677-682
68. Reck C, Florin E, Wojtecki L, Krause H, Groiss S, Voges J, Maarouf M, Sturm V, Schnitzler A, Timmermann L (2009) Characterisation of tremor-associated local field potentials in the subthalamic nucleus in Parkinson's disease. Eur J Neurosci 29:599-612
69. Shimizu M, Uno H, Ito T, Masuda Y, Kurokawa M (1996) Research and development of zonisamide, a new type of antiepileptic drug. Yakugaku Zassi 116(7):533-547 (Pubitemid 26257309)
70. Smith Y, Bevan MD, Shink E, Bolam JP (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86:353-387 (Pubitemid 28293917)
71. Steriade M, Jones EG, Llinas RR (1990) Thalamic oscillations and signalling. Wiley, New York
72. Steriade M, Jones EG, McCormick DA (1997) Thalamus. Elsevier Science, Oxford
73. Su PC, Tseng HM, Liu HM, Yen RF, Liou HH (2002) Subthalamotomy for advanced Parkinson disease. J Neurosurg 97:598-606 (Pubitemid 34994377)
74. Suzuki S, Kawakami K, Nishimura S, Watanabe Y, Yagi K, Miyamoto K, Seino M (1992) Zonisamide blocks T-type calcium channel in cultured neurons of rat cerebral cortex. Epilepsy Res 12(1):21-27
75. Tai C-H, Pan M-K, Lin J-J, Huang C-S, Yang Y-C, Kuo C-C (2012) Subthalamic discharges as a causal determinant of parkinsonian motor deficits. Ann Neurol 72(3):464-476
76. 2+ channels remedies locomotor deficits in a rat model of Parkinson disease. J Clin Invest 121(8):3289-3305
77. Timmermann L, Gross J, Dirks M, Volkmann J, Freund HJ, Schnitzler A (2003) The cerebral oscillatory network of parkinsonian resting tremor. Brain 126:199-212 (Pubitemid 36068570)
78. Tseng HM, Su PC, Liu HM, Liou HH, Yen RF (2007) Bilateral subthalamotomy for advanced Parkinson disease. Surg Neurol S1:43-51
79. Vila M, Périer C, Féger J, Yelnik J, Faucheux B, Ruberg M, Raisman-Vozari R, Agid Y, Hirsch EC (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 12:337-344 (Pubitemid 30068438)
80. Volkmann J, Joliot M, Mogilner A, Ioannides AA, Lado F, Fazzini E, Ribary U, Llinás R (1996) Central motor loop oscillations in parkinsonian resting tremor revealed by magnetoencephalography. Neurology 46:1359-1370 (Pubitemid 26159299)
81. Wichmann T, Bergman H, DeLong MR (1994) The primate subthalamic nucleus. I. Functional properties in intact animals. J Neurophysiol 72(2):494-506 (Pubitemid 24273559)
82. Wilensky AJ, Friel PN, Ojemann LM, Dodrill CB, McCormick KB, Levy RH (1985) Zonisamide in epilepsy: a pilot study. Epilepsia 26:212-220 (Pubitemid 15001187)
83. Yagi K, Seino M (1992) Methodological requirements for clinical trials in refractory epilepsies - our experience with zonisamide. Prog Neuropsychopharmacol Biol Psychiatry 16:79-85
84. Yin HH, Knowlton BJ (2006) The role of the basal ganglia in habit formation. Nat Rev Neurosci 7:464-476 (Pubitemid 44012286)