Cortically evoked long-lasting inhibition of pallidal neurons in a transgenic mouse model of dystonia

Journal of Neuroscience

Volumn 28, Issue 51, 2008, Pages 13967-13977

  Chiken, Satomi ^a   Shashidharan, Pullanipally ^b   Nambu, Atsushi ^a,c  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

Basal ganglia; Dystonia; Extracellular recording; Globus pallidus; Movement disorders; Transgenic mouse model

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; DYSTONIA; ELECTROMYOGRAM; EVOKED CORTICAL RESPONSE; GLOBUS PALLIDUS; MOTOR CORTEX; MOUSE; MUSCLE CONTRACTION; NERVE CELL INHIBITION; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; WAKEFULNESS; ACTION POTENTIAL; ANIMAL; BRAIN CORTEX; DISEASE MODEL; ELECTRODE; ELECTROMYOGRAPHY; ELECTROSTIMULATION; GENETICS; INNERVATION; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; SKELETAL MUSCLE;

ACTION POTENTIALS; ANIMALS; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; DYSTONIA; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; ELECTROMYOGRAPHY; GLOBUS PALLIDUS; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; NEURAL INHIBITION; NEURONS;

EID: 58149388201     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3834-08.2008     Document Type: Article

References (63)

1. Abeles M (1982) Quantification, smoothing, and confidence limits for single-units' histograms. J Neurosci Methods 5:317-325.
2. Aldridge JW, Gilman S (1991) The temporal structure of spike trains in the primate basal ganglia: afferent regulation of bursting demonstrated with precentral cerebral cortical ablation. Brain Res 543:123-138.
3. Berardelli A, Rothwell JC, Hallett M, Thompson PD, Manfredi M, Marsden CD (1998) The pathophysiology of primary dystonia. Brain 121:1195-1212.
4. Bergstrom DA, Bromley SD, Walters JR (1984) Dopamine agonists increase pallidal unit activity: attenuation by agonist pretreatment and anesthesia. Eur J Pharmacol 100:3-12.
5. Bressman SB (2004) Dystonia genotypes, phenotypes, and classification. Adv Neurol 94:101-107.
6. Chiken S, Tokuno H (2003) Ablation of striatal interneurons influences activities of entopeduncular neurons. Neuroreport 14:675-678.
7. Cohen LG, Hallett M (1988) Hand cramps: clinical features and electromyographic patterns in a focal dystonia. Neurology 38:1005-1012.
8. Dang MT, Yokoi F, McNaught KS, Jengelley TA, Jackson T, Li J, Li Y (2005) Generation and characterization of Dyt1 ΔGAG knock-in mouse as a model for early-onset dystonia. Exp Neurol 196:452-463.
9. Dang MT, Yokoi F, Pence MA, Li Y (2006) Motor deficits and hyperactivity in Dyt1 knockdown mice. Neurosci Res 56:470-474.
10. DeLong MR, Crutcher MD, Georgopoulos AP (1985) Primate globus pallidus and subthalamic nucleus: functional organization. J Neurophysiol 53:530-543.
11. Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212:76-88.
12. Elias S, Joshua M, Goldberg JA, Heimer G, Arkadir D, Morris G, Bergman H (2007) Statistical properties of pauses of the high-frequency discharge neurons in the external segment of the globus pallidus. J Neurosci 27:2525-2538.
13. Fahn S (1988) Concept and classification of dystonia. Adv Neurol 50:1-8.
14. Fahn S, Bressman SB, Marsden CD (1998) Classification of dystonia. Adv Neurol 78:1-10.
15. Farmer SF, Sheean GL, Mayston MJ, Rothwell JC, Marsden CD, Conway BA, Halliday DM, Rosenberg JR, Stephens JA (1998) Abnormal motor unit synchronization of antagonist muscles underlies pathological cocontraction in upper limb dystonia. Brain 121:801-814.
16. Gernert M, Bennay M, Fedrowitz M, Rehders JH, Richter A (2002) Altered discharge pattern of basal ganglia output neurons in an animal model of idiopathic dystonia. J Neurosci 22:7244-7253.
17. Grundmann K, Reischmann B, Vanhoutte G, Hübener J, Teismann P, Hauser TK, Bonin M, Wilbertz J, Horn S, Nguyen HP, Kuhn M, Chanarat S, Wolburg H, Van der Linden A, Riess O (2007) Overexpression of human wildtype torsinA and human ΔGAG torsinA in a transgenic mouse model causes phenotypic abnormalities. Neurobiol Dis 27:190-206.
18. Hamada I, DeLong MR (1992a) Excitotoxic acid lesions of the primate subthalamic nucleus result in transient dyskinesias of the contralateral limbs. J Neurophysiol 68:1850-1858.
19. Hamada I, DeLong MR (1992b) Excitotoxic acid lesions of the primate subthalamic nucleus result in reduced pallidal neuronal activity during active holding. J Neurophysiol 68:1859-1866.
20. Herz (1944) Dystonia. 1. Historical review: analysis of dystonic symptoms and physiologic mechanisms involved. Arch Neurol Psychiatry 51:305-318.
21. Inase M, Buford JA, Anderson ME (1996) Changes in the control of arm position, movement, and thalamic discharge during local inactivation in the globus pallidus of the monkey. J Neurophysiol 75:1087-1104.
22. Jedynak CP, Bonnet AM, Agid Y (1991) Tremor and idiopathic dystonia. Mov Disord 6:230-236.
23. Karmon B, Bergman H (1993) Detection of neuronal periodic oscillations in the basal ganglia of normal and parkinsonian monkeys. Isr J Med Sci 29:570-579.
24. Keane PE, Biziere K (1987) The effects of general anaesthetics on GABAergic synaptic transmission. Life Sci 41:1437-1448.
25. Kita H, Nambu A, Kaneda K, Tachibana Y, Takada M (2004) Role of ionotropic glutamatergic and GABAergic inputs on the firing activity of neurons in the external pallidum in awake monkeys. J Neurophysiol 92:3069-3084.
26. Kita H, Tachibana Y, Nambu A, Chiken S (2005) Balance of monosynaptic excitatory and disynaptic inhibitory responses of the globus pallidus induced after stimulation of the subthalamic nucleus in the monkey. J Neurosci 25:8611-8619.
27. B receptor-mediated responses of globus pallidus induced after stimulation of the putamen in the monkey. J Neurosci 26:6554-6562.
28. Kramer PL, Ozelius L, Brin MF, Fahn S, Kidd KK, Gusella J, Breakefield XO (1988) Molecular genetics of an autosomal dominant form of torsion dystonia. Adv Neurol 50:57-66.
29. Legéndy CR, Salcman M (1985) Bursts and recurrences of bursts in the spike trains of spontaneously active striate cortex neurons. J Neurophysiol 53:926-939.
30. Lenz FA, Suarez JI, Metman LV, Reich SG, Karp BI, Hallett M, Rowland LH, Dougherty PM (1998) Pallidal activity during dystonia: somatosensory reorganisation and changes with severity. J Neurol Neurosurg Psychiatry 65:767-770.
31. Liang F, Rouiller EM, Wiesendanger M (1993) Modulation of sustained electromyographic activity by single microstimuli: comparison of two forelimb motor cortical areas of the rat. Somatosens Mot Res 10:51-61.
32. Liu X, Tailor J, Wang S, Yianni J, Gregory R, Stein J, Aziz T (2004) Reversal of hypertonic co-contraction after bilateral pallidal stimulation in generalised dystonia: a clinical and electromyogram case study. Mov Disord 19:336-340.
33. Löscher W, Rohlfs A, Rundfeldt C (1995) Reduction in firing rate of substantia nigra pars reticulata neurons by valproate: influence of different types of anesthesia in rats. Brain Res 702:133-144.
34. Marsden CD, Rothwell JC (1987) The physiology of idiopathic dystonia. Can J Neurol Sci 14:521-527.
35. Maurice N, Deniau JM, Glowinski J, Thierry AM (1998) Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the corticosubthalamic circuits. J Neurosci 18:9539-9546.
36. Maurice N, Deniau JM, Glowinski J, Thierry AM (1999) Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the cortico-nigral circuits. J Neurosci 19:4674-4681.
37. Mink JW, Thach WT (1991) Basal ganglia motor control. III. Pallidal ablation: normal reaction time, muscle cocontraction, and slow movement. J Neurophysiol 65:330-351.
38. Nambu A, Yoshida S, Jinnai K (1990) Discharge patterns of pallidal neurons with input from various cortical areas during movement in the monkey. Brain Res 519:183-191.
39. 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 84:289-300.
40. Nambu A, Tokuno H, Takada M (2002) Functional significance of the cortico-subthalamo-pallidal "hyperdirect" pathway. Neurosci Res 43:111-117.
41. Neafsey EJ, Sievert C (1982) A second forelimb motor area exists in rat frontal cortex. Brain Res 232:151-156.
42. Neafsey EJ, Bold EL, Hass G, Hurley-Gius KM, Guirk G, Sievert CF, Terreberry RR (1986) The organization of the rat motor cortex: a microstimulation mapping study. Brain Res Rev 11:77-96.
43. Obeso JA, Rothwell JC, Lang AE, Marsden CD (1983) Myoclonic dystonia. Neurology 33:825-830.
44. Ozelius LJ, Hewett J, Kramer P, Bressman SB, Shalish C, de Leon D, Rutter M, Risch N, Brin MF, Markova ED, Limborska SA, Ivanova-Smolenskaya IA, McCormick MK, Fahn S, Buckler AJ, Gusella JF, Breakefield XO (1997a) Fine localization of the torsion dystonia gene (DYT1) on human chromosome 9q34: YAC map and linkage disequilibrium. Genome Res 7:483-494.
45. Ozelius LJ, Hewett JW, Page CE, Bressman SB, Kramer PL, Shalish C, de Leon D, Brin MF, Raymond D, Corey DP, Fahn S, Risch NJ, Buckler AJ, Gusella JF, Breakefield XO (1997b) The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat Genet 17:40-48.
46. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
47. Robertson RG, Farmery SM, Sambrook MA, Crossman AR (1989) Dyskinesia in the primate following injection of an excitatory amino acid antagonist into the medial segment of the globus pallidus. Brain Res 476:317-322.
48. Rouiller EM, Moret V, Liang F (1993) Comparison of the connection properties of the two forelimb areas of the rat sensorimotor cortex: support for the presence of a premotor or supplementary motor cortical area. Somatosens Mot Res 10:269-289.
49. Ryan LJ, Sanders DJ (1994) Subthalamic nucleus and globus pallidus lesions alter activity in nigrothalamic neurons in rats. Brain Res Bull 34:19-26.
50. Sanger TD, Tarsy D, Pascual-Leone A (2001) Abnormalities of spatial and temporal sensory discrimination in writer's cramp. Mov Disord 16:94-99.
51. Sharma N, Baxter MG, Petravicz J, Bragg DC, Schienda A, Standaert DG, Breakefield XO (2005) Impaired motor learning in mice expressing torsinA with the DYT1 dystonia mutation. J Neurosci 25:5351-5355.
52. Shashidharan P, Sandu D, Potla U, Armata IA, Walker RH, McNaught KS, Weisz D, Sreenath T, Brin MF, Olanow CW (2005) Transgenic mouse model of early-onset DYT1 dystonia. Hum Mol Genet 14:125-133.
53. Starr PA, Rau GM, Davis V, Marks WJ Jr, Ostrem JL, Simmons D, Lindsey N, Turner RS (2005) Spontaneous pallidal neuronal activity in human dystonia: comparison with Parkinson's disease and normal macaque. J Neurophysiol 93:3165-3176.
54. Tachibana Y, Kita H, Chiken S, Takada M, Nambu A (2008) Motor cortical control of internal pallidal activity through glutamatergic and GABAergic inputs in awake monkeys. Eur J Neurosci 27:238-253.
55. Tang JK, Moro E, Mahant N, Hutchison WD, Lang AE, Lozano AM, Dostrovsky JO (2007) Neuronal firing rates and patterns in the globus pallidus internus of patients with cervical dystonia differ from those with Parkinson's disease. J Neurophysiol 98:720-729.
56. Vitek JL (2002) Pathophysiology of dystonia: a neuronal model. Mov Disord 17 [Suppl 3]:S49-S62.
57. Vitek JL, Chockkan V, Zhang JY, Kaneoke Y, Evatt M, DeLong MR, Triche S, Mewes K, Hashimoto T, Bakay RA (1999) Neuronal activity in the basal ganglia in patients with generalized dystonia and hemiballismus. Ann Neurol 46:22-35.
58. 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 95:2120-2133.
59. Yanagisawa N, Goto A (1971) Dystonia musculorum deformans. Analysis with electromyography. J Neurol Sci 13:39-65.
60. Yasoshima Y, Kai N, Yoshida S, Shiosaka S, Koyama Y, Kayama Y, Kobayashi K (2005) Subthalamic neurons coordinate basal ganglia function through differential neural pathways. J Neurosci 25:7743-7753.
61. Yoshida S, Nambu A, Jinnai K (1993) The distribution of the globus pallidus neurons with input from various cortical areas in the monkeys. Brain Res 611:170-174.
62. Zhao Y, DeCuypere M, LeDoux MS (2008) Abnormal motor function and dopamine neurotransmission in DYT1 ΔGAG transgenic mice. Exp Neurol 210:719-730.
63. Zhuang P, Li Y, Hallett M (2004) Neuronal activity in the basal ganglia and thalamus in patients with dystonia. Clin Neurophysiol 115:2542-2557.