Enhanced Synchrony among Primary Motor Cortex Neurons in the 1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine Primate Model of Parkinson's Disease

Journal of Neuroscience

Volumn 22, Issue 11, 2002, Pages 4639-4653

  Goldberg, Joshua A ^a   Boraud, Thomas ^a   Maraton, Sharon ^a   Haber, Suzanne N ^b   Vaadia, Eilon ^a   Bergman, Hagai ^a  

^a HEBREW UNIVERSITY   (Israel)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Correlations; EMG; Firing patterns; Globus pallidus; Intracortical microstimulation; Kinesthetic; Monkey; Neuronal synchronization; Oscillations; Striatum

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; DOPAMINE RECEPTOR STIMULATING AGENT; TYROSINE 3 MONOOXYGENASE;

ACCELEROMETER; AKINESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN NERVE CELL; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; ELECTROMYOGRAPHY; FEMALE; FORELIMB; GLOBUS PALLIDUS; IMMOBILIZATION; MOTOR CORTEX; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RIGIDITY; ACTION POTENTIAL; ANIMAL; ARM; BIOMECHANICS; BIOSYNTHESIS; CERCOPITHECUS; CHEMICALLY INDUCED DISORDER; CORPUS STRIATUM; DISEASE COURSE; DISEASE MODEL; DRUG EFFECT; ELECTROSTIMULATION; IMMUNOHISTOCHEMISTRY; JOINT CHARACTERISTICS AND FUNCTIONS; MACACA; METHODOLOGY; MOTOR PERFORMANCE; MUSCLE RIGIDITY; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ACTION POTENTIALS; ANIMALS; ARM; BIOMECHANICS; CERCOPITHECUS AETHIOPS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOPAMINE AGENTS; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; FEMALE; GLOBUS PALLIDUS; IMMUNOHISTOCHEMISTRY; MACACA FASCICULARIS; MOTOR CORTEX; MOTOR SKILLS; MUSCLE RIGIDITY; NEURONS; PARKINSON DISEASE, SECONDARY; RANGE OF MOTION, ARTICULAR; TYROSINE 3-MONOOXYGENASE;

EID: 0036615887     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-11-04639.2002     Document Type: Article

References (96)

1. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-375.
2. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381.
3. Arthurs OJ, Boniface S (2002) How well do we understand the neural origins of the fMRI BOLD signal? Trends Neurosci 25:27-31.
4. Asanuma H (1989) The motor cortex. New York: Raven.
5. Bar-Gad I, Ritov Y, Vaadia E, Bergman H (2001) Failure in identification of overlapping spikes from multiple neuron activity causes artificial correlations. J Neurosci Methods 107:1-13.
6. Basmajian JV, De Luca CJ (1985) Muscles alive: their function revealed by electromyography. Baltimore: Williams & Wilkins.
7. Bauswein E, Fromm C, Preuss A (1989) Corticostriatal cells in comparison with pyramidal tract neurons: contrasting properties in the behaving monkey. Brain Res 493:198-203.
8. Benazzouz A, Gross C, Dupont J, Bioulac B (1992) MPTP induced hemiparkinsonism in monkeys: behavioral, mechanographic, electromyographic and immunohistochemical studies. Exp Brain Res 90:116-120.
9. Benazzouz A, Boraud T, Dubedat P, Boireau A, Stutzmann JM, Gross C (1995) Riluzole prevents MPTP-induced parkinsonism in the rhesus monkey: a pilot study. Eur J Pharmacol 284:299-307.
10. Bergman H, Wichmann T, Karmon B, DeLong MR (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72:507-520.
11. Bergman H, Feingold A, Nini A, Raz A, Slovin H, Abeles M, Vaadia E (1998) Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci 21:32-38.
12. Bezard E, Boraud T, Bioulac B, Gross CE (1999) Involvement of the subthalamic nucleus in glutamatergic compensatory mechanisms. Eur J Neurosci 11:2167-2170.
13. Bolam JP, Hanley JJ, Booth PA, Bevan MD (2000) Synaptic organisation of the basal ganglia. J Anat 196:527-542.
14. Boraud T, Bezard E, Guehl D, Bioulac B, Gross C (1998) Effects of L-DOPA on neuronal activity of the globus pallidus externalis (GPe) and globus pallidus internalis (GPi) in the MPTP-treated monkey. Brain Res 787:157-160.
15. Boraud T, Bezard E, Bioulac B, Gross CE (2000) Ratio of inhibited-to-activated pallidal neurons decreases dramatically during passive limb movement in the MPTP-treated monkey. J Neurophysiol 83:1760-1763.
16. Boraud T, Bezard E, Bioulac B, Gross CE (2001) Dopamine agonist-induced dyskinesias are correlated to both firing pattern and frequency alterations of pallidal neurones in the MPTP-treated monkey. Brain 124:546-557.
17. Boraud T, Bezard E, Bioulac B, Gross CE (2002) From single extracellular unit recording in experimental and human parkinsonism to the development of a functional concept of the role played by the basal ganglia in motor control. Prog Neurobiol 66:265-283.
18. Brown P (2000) Cortical drives to human muscle: the Piper and related rhythms. Prog Neurobiol 60:97-108.
19. Brown P, Marsden CD (1999) Bradykinesia and impairment of EEG desynchronization in Parkinson's disease. Mov Disord 14:423-429.
20. Brown P, Salenius S, Rothwell JC, Hari R (1998) Cortical correlate of the Piper rhythm in humans. J Neurophysiol 80:2911-2917.
21. Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, Di Lazzaro V (2001) Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J Neurosci 21:1033-1038.
22. Carpenter AF, Georgopoulos AP, Pellizzer G (1999) Motor cortical encoding of serial order in a context-recall task. Science 283:1752-1757.
23. Ceballos-Baumann AO, Obeso JA, Vitek JL, DeLong MR, Bakay R, Linazasoro G, Brooks DJ (1994) Restoration of thalamocortical activity after posteroventral pallidotomy in Parkinson's disease. Lancet 344:814.
24. Ceballos-Baumann AO, Boecker H, Bartenstein P, von Falkenhayn I, Riescher H, Conrad B, Moringlane JR, Alesch F (1999) A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Arch Neurol 56:997-1003.
25. DeLong MR (1971) Activity of pallidal neurons during movement. J Neurophysiol 34:414-427.
26. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281-285.
27. Dick JP, Cowan JM, Day BL, Berardelli A, Kachi T, Rothwell JC, Marsden CD (1984) The corticomotoneurone connection is normal in Parkinson's disease. Nature 310:407-409.
28. Doudet DJ, Gross C, Arluison M, Bioulac B (1990) Modifications of precentral cortex discharge and EMG activity in monkeys with MPTP-induced lesions of DA nigral neurons. Exp Brain Res 80:177-188.
29. Eidelberg D, Moeller JR, Ishikawa T, Dhawan V, Spetsieris P, Silbersweig D, Stern E, Woods RP, Fazzini E, Dogali M, Beric A (1996) Regional metabolic correlates of surgical outcome following unilateral pallidotomy for Parkinson's disease. Ann Neurol 39:450-459.
30. Evarts EV (1964) Temporal patterns of discharge of pyramidal tract neurons during sleep and waking in the monkey. J Neurophysiol 27:152-171.
31. Evarts EV (1965) Relation of discharge frequency to conduction velocity in pyramidal tract neurons. J Neurophysiol 28:216-228.
32. Fee MS, Mitra PP, Kleinfeld D (1996) Variability of extracellular spike waveforms of cortical neurons. J Neurophysiol 76:3823-3833.
33. Filion M, Tremblay L (1991) Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res 547:142-151.
34. Filion M, Tremblay L, Bedard PJ (1988) Abnormal influences of passive limb movement on the activity of globus pallidus neurons in parkinsonian monkeys. Brain Res 444:165-176.
35. Freeman A, Ciliax B, Bakay R, Daley J, Miller RD, Keating G, Levey A, Rye D (2001) Nigrostriatal collaterals to thalamus degenerate in parkinsonian animal models. Ann Neurol 50:321-329.
36. Fukuda M, Mentis M, Ghilardi MF, Dhawan V, Antonini A, Hammerstad J, Lozano AM, Lang A, Lyons K, Koller W, Ghez C, Eidelberg D (2001) Functional correlates of pallidal stimulation for Parkinson's disease. Ann Neurol 49:155-164.
37. Gerfen CR, Wilson CJ (1996) The basal ganglia. In: Handbook of chemical neuroanatomy, Vol 12: Integrated systems of the CNS, Part III (Swanson LW, Bjorklund A, Hokfelt T, eds), pp 371-468. New York: Elsevier Science.
38. Goldberg JA, Boraud T, Maraton S, Vaadia E, Bergman H (2002) Enhanced synchrony in the primary motor cortex of MPTP primates may underlie muscle cocontraction and rigidity. In: The basal ganglia VII (Nicholson LFB, Faull RLM, eds), New York: Plenum, in press.
39. Grafton ST, Waters C, Sutton J, Lew MF, Couldwell W (1995) Pallidotomy increases activity of motor association cortex in Parkinson's disease: a positron emission tomographic study. Ann Neurol 37:776-783.
40. Graybiel AM, Aosaki T, Flaherty AW, Kimura M (1994) The basal ganglia and adaptive motor control. Science 265:1826-1831.
41. Gross C, Feger J, Seal J, Haramburu P, Bioulac B (1983) Neuronal activity in area 4 and movement parameters recorded in trained monkeys after unilateral lesion of the substantia nigra. Exp Brain Res [Suppl] 7:181-193.
42. Gross CE, Boraud T, Guehl D, Bioulac B, Bezard E (1999) From experimentation to the surgical treatment of Parkinson's disease: prelude or suite in basal ganglia research? Prog Neurobiol 59:509-532.
43. Gur M, Beylin A, Snodderly DM (1999) Physiological properties of macaque V1 neurons are correlated with extracellular spike amplitude, duration, and polarity. J Neurophysiol 82:1451-1464.
44. Haslinger B, Erhard P, Kampfe N, Boecker H, Rummeny E, Schwaiger M, Conrad B, Ceballos-Baumann AO (2001) Event-related functional magnetic resonance imaging in Parkinson's disease before and after levodopa. Brain 124:558-570.
45. Heeger DJ, Huk AC, Geisler WS, Albrecht DG (2000) Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? Nat Neurosci 3:631-633.
46. Henselmans JM, de Jong BM, Pruim J, Staal MJ, Rutgers AW, Haaxma R (2000) Acute effects of thalamotomy and pallidotomy on regional cerebral metabolism, evaluated by PET. Clin Neurol Neurosurg 102:84-90.
47. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427-442.
48. Hoover JE, Strick PL (1999) The organization of cerebellar and basal ganglia outputs to primary motor cortex as revealed by retrograde transneuronal transport of herpes simplex virus type 1. J Neurosci 19:1446-1463.
49. 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 USA 96:1674-1679.
50. Imbert C, Bezard E, Guitraud S, Boraud T, Gross CE (2000) Comparison of eight clinical rating scales used for the assessment of MPTP-induced parkinsonism in the Macaque monkey. J Neurosci Methods 96:71-76.
51. Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects. Brain 118:913-933.
52. Jueptner M, Weiller C (1995) Review: does measurement of regional cerebral blood flow reflect synaptic activity? Implications for PET and fMRI. NeuroImage 2:148-156.
53. Kaneoke Y, Vitek JL (1996) Burst and oscillation as disparate neuronal properties. J Neurosci Methods 68:211-223.
54. Kimura M, Rajkowski J, Evarts E (1984) Tonically discharging putamen neurons exhibit set-dependent responses. Proc Natl Acad Sci USA 81:4998-5001.
55. Kleine BU, Praamstra P, Stegeman DF, Zwarts MJ (2001) Impaired motor cortical inhibition in Parkinson's disease: motor unit responses to transcranial magnetic stimulation. Exp Brain Res 138:477-483.
56. Lavoie B, Parent A (1991) Dopaminergic neurons expressing calbindin in normal and parkinsonian monkeys. NeuroReport 2:601-604.
57. Levy R, Hutchison WD, Lozano AM, Dostrovsky JO (2000) High-frequency synchronization of neuronal activity in the subthalamic nucleus of parkinsonian patients with limb tremor. J Neurosci 20:7766-7775.
58. Limousin P, Greene J, Pollak P, Rothwell J, Benabid AL, Frackowiak R (1997) Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson's disease. Ann Neurol 42:283-291.
59. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150-157.
60. Lynd BE, Haber SN (1994) The organization of midbrain projections to the striatum in the primate: sensorimotor-related striatum versus ventral striatum. Neuroscience 59:625-640.
61. Magill PJ, Bolam JP, Bevan MD (2000) Relationship of activity in the subthalamic nucleus-globus pallidus network to cortical electroencephalogram. J Neurosci 20:820-833.
62. Marsden CD, Obeso JA (1994) The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's disease. Brain 117:877-897.
63. Marsden JF, Limousin-Dowsey P, Ashby P, Pollak P, Brown P (2001) Subthalamic nucleus, sensorimotor cortex and muscle interrelationship in Parkinson's disease. Brain 124:378-388.
64. Miller WC, DeLong MR (1987) Altered tonic activity of neurons in the globus pallidus and subthalamic nucleus in the primate MPTP model of parkinsonism. In: The basal ganglia II (Carpenter MB, Jayaraman A, eds), pp 415-427. New York: Plenum.
65. Muir RB, Lemon RN (1983) Corticospinal neurons with a special role in precision grip. Brain Res 261:312-316.
66. Munro-Davies LE, Winter J, Aziz TZ, Stein JF (1999) The role of the pedunculopontine region in basal-ganglia mechanisms of akinesia. Exp Brain Res 129:511-517.
67. Murthy VN, Fetz EE (1996) Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. J Neurophysiol 76:3968-3982.
68. Nini A, Feingold A, Slovin H, Bergman H (1995) Neurons in the globus pallidus do not show correlated activity in the normal monkey, but phase-locked oscillations appear in the MPTP model of parkinsonism. J Neurophysiol 74:1800-1805.
69. Obeso JA, Rodriguez-Oroz MC, Rodriguez M, DeLong MR, Olanow CW (2000) Pathophysiology of levodopa-induced dyskinesias in Parkinson's disease: problems with the current model. Ann Neurol 47:S22-S32.
70. Ohara S, Mima T, Baba K, Ikeda A, Kuneida T, Matsumo R, Yamamoto J, Matsuhashi M, Nagamine T, Hirasawa K, Hori T, Mihara T, Hashimoto N, Salenius S, Shibasaki H (2001) Increased synchronization of cortical oscillatory activities between human supplementary motor and primary sensorimotor areas during voluntary movements. J Neurosci 21:9377-9386.
71. Pahapill PA, Lozano AM (2000) The pedunculopontine nucleus and Parkinson's disease. Brain 123:1767-1783.
72. Phillips CJ, Porter R (1977) Corticospinal neurones: their role in movement. London: Academic.
73. Playford ED, Jenkins IH, Passingham RE, Nutt J, Frackowiak RS, Brooks DJ (1992) Impaired mesial frontal and putamen activation in Parkinson's disease: a positron emission tomography study. Ann Neurol 32:151-161.
74. Plenz D, Kitai ST (1999) A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400:677-682.
75. Porrino LJ, Burns RS, Crane AM, Palombo E, Kopin IJ, Sokoloff L (1987) Changes in local cerebral glucose utilization associated with Parkinson's syndrome induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in the primate. Life Sci 40:1657-1664.
76. Porter R, Lemon RN (1993) Corticospinal function and voluntary movement. New York: Oxford UP.
77. Rascol O, Sabatini U, Chollet F, Fabre N, Senard JM, Montastruc JL, Celsis P, Marc-Vergnes JP, Rascol A (1994) Normal activation of the supplementary motor area in patients with Parkinson's disease undergoing long-term treatment with levodopa. J Neurol Neurosurg Psychiatry 57:567-571.
78. Raz A, Feingold A, Zelanskaya V, Vaadia E, Bergman H (1996) Neuronal synchronization of tonically active neurons in the striatum of normal and parkinsonian primates. J Neurophysiol 76:2083-2088.
79. Raz A, Vaadia E, Bergman H (2000) Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine vervet model of parkinsonism. J Neurosci 20:8559-8571.
80. Ridding MC, Inzelberg R, Rothwell JC (1995) Changes in excitability of motor cortical circuitry in patients with Parkinson's disease. Ann Neurol 37:181-188.
81. Rothblat DS, Schneider JS (1993) Response of caudate neurons to stimulation of intrinsic and peripheral afferents in normal, symptomatic, and recovered MPTP-treated cats. J Neurosci 13:4372-4378.
82. Rothblat DS, Schneider JS (1995) Alterations in pallidal neuronal responses to peripheral sensory and striatal stimulation in symptomatic and recovered parkinsonian cats. Brain Res 705:1-14.
83. Rothwell JC (1999) Pathophysiology of the motor cortex in patients with Parkinson's disease. Adv Neurol 80:27-29.
84. Sabatini U, Boulanouar K, Fabre N, Martin F, Carel C, Colonnese C, Bozzao L, Berry I, Montastruc JL, Chollet F, Rascol O (2000) Cortical motor reorganization in akinetic patients with Parkinson's disease: a functional MRI study. Brain 123:394-403.
85. Samuel M, Ceballos BA, Blin J, Uema T, Boecker H, Passingham RE, Brooks DJ (1997a) Evidence for lateral premotor and parietal over-activity in Parkinson's disease during sequential and bimanual movements. A PET study. Brain 120:963-976.
86. Samuel M, Ceballos BA, Turjanski N, Boecker H, Gorospe A, Linazasoro G, Holmes AP, DeLong MR, Vitek JL, Thomas DG, Quinn NP, Obeso JA, Brooks DJ (1997b) Pallidotomy in Parkinson's disease increases supplementary motor area and prefrontal activation during performance of volitional movements: an H2(15)O PET study. Brain 120:1301-1313.
87. Schwartzman RJ, Alexander GM, Ferraro TN, Grothusen JR, Stahl SM (1988) Cerebral metabolism of parkinsonian primates 21 days after MPTP. Exp Neurol 102:307-313.
88. Song DD, Haber SN (2000) Striatal responses to partial dopaminergic lesion: evidence for compensatory sprouting. J Neurosci 20:5102-5114.
89. Thobois S, Dominey P, Decety J, Pollak P, Gregoire MC, Broussolle E (2000) Overactivation of primary motor cortex is asymmetrical in hemiparkinsonian patients. NeuroReport 11:785-789.
90. Tokuno H, Nambu A (2000) Organization of nonprimary motor cortical inputs on pyramidal and nonpyramidal tract neurons of primary motor cortex: an electrophysiological study in the macaque monkey. Cereb Cortex 10:58-68.
91. Tremblay L, Filion M, Bedard PJ (1989) Responses of pallidal neurons to striatal stimulation in monkeys with MPTP-induced parkinsonism. Brain Res 498:17-33.
92. Turner RS, DeLong MR (2000) Corticostriatal activity in primary motor cortex of the macaque. J Neurosci 20:7096-7108.
93. Vitek JL, Giroux M (2000) Physiology of hypokinetic and hyperkinetic movement disorders: model for dyskinesia. Ann Neurol 47:S131-S140.
94. Wang HC, Lees AJ, Brown P (1999) Impairment of EEG desynchronization before and during movement and its relation to bradykinesia in Parkinson's disease. J Neurol Neurosurg Psychiatry 66:442-446.
95. Watts RL, Mandir AS (1992) The role of motor cortex in the pathophysiology of voluntary movement deficits associated with parkinsonism. Neurol Clin 10:451-469.
96. Wichmann T, Bergman H, Starr PA, Subramanian T, Watts RL, DeLong MR (1999) 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 125:397-409.