Competition between feedback loops underlies normal and pathological dynamics in the basal ganglia

Journal of Neuroscience

Volumn 26, Issue 13, 2006, Pages 3567-3583

  Leblois, Arthur ^a,c   Boraud, Thomas ^a,c   Meissner, Wassilios ^a   Bergman, Hagai ^b,c   Hansel, David ^a,c,d  

^a CNRS   (France)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d Laboratoire de Neurophysique et Physiologie du Système Moteur   (France)

Author keywords

Action selection; Models; Neural network; Oscillations; Parkinson's disease; Synchrony

Indexed keywords

DOPAMINE;

ARTICLE; BASAL GANGLION; BRAIN CORTEX; CORPUS STRIATUM; FEEDBACK SYSTEM; GLOBUS PALLIDUS; MODEL; MOTOR CORTEX; OSCILLATION; PATHOLOGY; PRIORITY JOURNAL; SUBTHALAMIC NUCLEUS; SYNAPTIC TRANSMISSION; THALAMUS;

ACTION POTENTIALS; ANIMALS; BASAL GANGLIA; BIOLOGICAL CLOCKS; BRAIN; COMPUTER SIMULATION; DOPAMINE; FEEDBACK; HUMANS; MODELS, NEUROLOGICAL; MOVEMENT; NERVE NET; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONS; PARKINSON DISEASE;

EID: 33645452258     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5050-05.2006     Document Type: Article

References (85)

1. Aizman O, Brismar H, Uhlen P, Zettergren E, Levey AI, Forssberg H, Greengard P, Aperia A (2000) Anatomical and physiological evidence for D1 and D2 dopamine receptor colocalization in neostriatal neurons. Nat Neurosci 3:226-230.
2. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-375.
3. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381.
4. Apicella P, Ljungberg T, Scarnati E, Schultz W (1991) Responses to reward in monkey dorsal and ventral striatum. Exp Brain Res 85:491-500.
5. Baker SN, Gerstein GL (2001) Determination of response latency and its application to normalization of cross-correlation measures. Neural Comput 13:1351-1377.
6. Bar-Gad I, Bergman H (2001) Stepping out of the box: information processing in the neural networks of the basal ganglia. Curr Opin Neurobiol 11:689-695.
7. Beiser DG, Houk JC (1998) Model of cortical-basal ganglionic processing: encoding the serial order of sensory events. J Neurophysiol 79:3168-3188.
8. Benazzouz A, Gross C, Feger J, Boraud T, Bioulac B (1993) Reversal of rigidity and improvement in motor performance by subthalamic highfrequency stimulation in MPTP-treated monkeys. Eur J Neurosci 5:382-389.
9. Bergman H, Wichmann T, DeLong MR (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249:1436-1438.
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. Bevan MD, Wilson CJ (1999) Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J Neurosci 19:7617-7628.
12. Bolam JP, Hanley JJ, Booth PAC, Bevan MD (2000) Synaptic organisation of the basal ganglia. J Anat 196:527-542.
13. Boraud T, Bezard E, Bioulac B, Gross CE (2000) Ratio of inhibited-toactivated pallidal neurons decreases dramatically during passive limb movement in the MPTP-treated monkey. J Neurophysiol 83:1760-1763.
14. 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.
15. Boussaoud D, Kermadi I (1997) The primate striatum: neuronal activity in relation to spatial attention versus motor preparation. Eur J Neurosci 9:2152-2168.
16. Brotchie JM, Iansek R, Horne MK (1991) Motor function of the monkey globus pallidus. I. Neuronal discharge and parameters of movements. Brain 114:1667-1683.
17. 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.
18. Calabresi P, Centonze D, Bernardi G (2000) Electrophysiology of dopamine in normal and denervated striatal neurons. Trends Neurosci 23:S57-S63.
19. Chevalier G, Deniau JM (1990) Disinhibition as basic process in the expression in striatal functions. Trends Neurosci 13:277-280.
20. Cossette M, Levesque M, Parent A (1999) Extrastriatal dopaminergic innervation of human basal ganglia. Neurosci Res 34:51-54.
21. DeLong MR (1990) Primate models of movement disorders of basal ganglia. Trends Neurosci 13:281-285.
22. Deniau JM (1985) Disinhibition as a basic process in the expression of striatal functions. II. The striato-nigral influence on thalamocortical cells of the ventromedial thalamic nucleus. Brain Res 334:227-233.
23. Deniau JM, Lackner D, Feger J (1978) Effect of substantia nigra stimulation on identified neurons in the VL-VA thalamic complex: comparison between intact and chronically decorticated cats. Brain Res 145:27-35.
24. Deniau JM, Menetrey A, Charpier S (1996) The lamellar organization of the rat substantia nigra pars reticulata: segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections. Neuroscience 73:761-781.
25. Ermentrout B (1996) Type I membranes, phase resetting curves, and synchrony. Neural Comput 8:979-1001.
26. 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.
27. Gardiner TW, Nelson RJ (1992) Striatal neuronal activity during the initiation and execution of hand movements made in response to visual and vibratory cues. Exp Brain Res 92:15-26.
28. Gerfen CR, Wilson CJ (1996) The basal ganglia. In: Handbook of chemical neuroanatomy, Vol 12, Integrated systems of the CNS, Pt III (Swanson LW, Bjorklund A, Hokfelt T, eds), pp 371-468. Amsterdam: Elsevier.
29. Goldberg JA, Hansel D, Bergman H, Sompolinsky H (1999) Network model of parkinsonian neuronal oscillations in the cortico-basal ganglionic circuit. Soc Neurosci Abstr 25:765.3.
30. Goldberg JA, Boraud T, Maraton S, Haber SN, Vaadia E, Bergman H (2002) Enhanced synchrony among primary motor cortex neurons in the MPTP primate model of Parkinson's disease. J Neurosci 22:4639-4953.
31. Golomb D, Hansel D (2000) The number of synaptic inputs and the synchrony of large, sparse neuronal networks. Neural Comput 12:1095-1139.
32. Graybiel AM (2000) The basal ganglia. Curr Biol 10:R509-R511.
33. Gurney K, Prescott TJ, Redgrave P (2001a) A computational model of action selection in the basal ganglia. I. A new functional anatomy. Biol Cybern 84:401-410.
34. Gurney K, Prescott TJ, Redgrave P (2001b) A computational model of action selection in the basal ganglia. II. Analysis and simulation of behaviour. Biol Cybern 84:411-423.
35. Haber SN, Fudge JL (1997) The primate substantia nigra and VTA: integrative circuitry and function. Crit Rev Neurobiol 11:323-342.
36. Halliday DM, Rosenberg JR (2000) On the application, estimation and interpretation of coherence and pooled coherence. J Neurosci Methods 100:173-174.
37. 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.
38. Hoover JE, Strick PL (1993) Multiple output channels in the basal ganglia. Science 259:819-821.
39. 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.
40. Hopfield JJ (1984) Neurons with graded response have collective computational properties like those of two-state neurons. Proc Natl Acad Sci USA 81:3088-3092.
41. Hutchison WD, Lozano AM, Tasker RR, Lang AE, Dostrovsky JO (1997) Identification and characterization of neurons with tremor-frequency activity in human globus pallidus. Exp Brain Res 113:557-563.
42. Hutchison WD, Dostrovsky JO, Walters JR, Courtemanche R, Boraud T, Goldberg J, Brown P (2004) Neuronal oscillations in the basal ganglia and movement disorders: evidence from whole animal and human recordings. J Neurosci 24:9240-9243.
43. Jaeger D, Kita H, Wilson CJ (1994) Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. J Neurophysiol 72:2555-2558.
44. Kayahara T, Nakano K (1996) Pallido-thalamo-motor cortical connections: an electron microscopic study in the macaque monkey. Brain Res 706:337-342.
45. Kelly RM, Strick PL (2004) Macro-architecture of basal ganglia loops with the cerebral cortex: use of rabies virus to reveal multisynaptic circuits. Prog Brain Res 143:449-459.
46. Kerr JN, Wickens JR (2001) Dopamine D-1/D-5 receptor activation is required for long-term potentiation in the rat neostriatum in vitro. J Neurophysiol 85:117-124.
47. Kincaid AE, Zheng T, Wilson CJ (1998) Connectivity and convergence of single corticostriatal axons. J Neurosci 18:4722-4731.
48. Kish LJ, Palmer MR, Gerhardt GA (1999) Multiple single-unit recordings in the striatum of freely moving animals: effects of apomorphine and D-amphetamine in normal and unilateral 6-hydroxydopamine-lesioned rats. Brain Res 833:58-70.
49. Kiyatkin EA, Rebec GV (1996) Dopaminergic modulation of glutamateinduced excitations of neurons in the neostriatum and nucleus accumbens of awake, unrestrained rats. J Neurophysiol 75:142-153.
50. Leblois A, Boraud T, Bergman H, Hansel D (2002) A model of the basal ganglia physiology and pathophysiology built on competition between direct and hyperdirect pathways. Soc Neurosci Abstr 28:915.11.
51. Leblois A, Boraud T, Bergman H, Hansel D (2003) The roles of feedback loops in the physiology and physiopathology of the basal ganglia. Soc Neurosci Abstr 29:358.1.
52. Lee IH, Assad JA (2003) Putaminal activity for simple reactions or self-timed movements. J Neurophysiol 89:2528-2537.
53. Levesque M, Parent A (2005) The striatofugal fiber system in primates: a reevaluation of its organization based on single-axon tracing studies. Proc Natl Acad Sci USA 102:11888-11893.
54. Levy R, Ashby P, Hutchison WD, Lang AE, Lozano AM, Dostrovsky JO (2002) Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson's disease. Brain 125:1196-1209.
55. 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.
56. Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381-425.
57. Mink JW, Thach WT (1991) Basal ganglia motor control. II. Late pallidal timing relative to movement onset and inconsistent pallidal coding of movement parameters. J Neurophysiol 65:301-329.
58. Mink JW, Thach WT (1993) Basal ganglia intrinsic circuits and their role in behavior. Curr Opin Neurobiol 3:950-957.
59. Nakano K (2000) Neural circuits and topographic organization of the basal ganglia and related regions. Brain Dev 22:S5-S16.
60. Nambu A, Tokuno H, Hamada I, Kita H, Imanishi M, Akazawa T, Ikeuchi Y, Asegawa N (2000) Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J Neurophysiol 84:289-300.
61. Nicola SM, Woodward Hopf F, Hjelmstad GO (2004) Contrast enhancement: a physiological effect of striatal dopamine? Cell Tissue Res 318:93-106.
62. 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.
63. O'Donnell P (2003) Dopamine gating of forebrain neural ensembles. Eur J Neurosci 17:429-435.
64. Parent A, Hazrati LN (1995a) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev 20:91-127.
65. Parent A, Hazrati LN (1995b) Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum. Brain Res Brain Res Rev 20:128-154.
66. Pessiglione M, Guehl D, Rolland AS, Francois C, Hirsch EC, Feger J, Tremblay L (2005) Thalamic neuronal activity in dopamine-depleted primates: evidence for a loss of functional segregation within basal ganglia circuits. J Neurosci 25:1523-1531.
67. Plenz D, Kitai ST (1998) Regulation of the nigrostriatal pathway by metabotropic glutamate receptors during development. J Neurosci 18:4133-4144.
68. Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1993) Numerical recipes in C, Ed 2. Cambridge, UK: Cambridge UP.
69. Raz A, Vaadia E, Bergman H (2000) Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous MPTP-treated vervet model of Parkinsonism. J Neurosci 20:8559-8571.
70. Raz A, Frechter-Mazar V, Feingold A, Abeles M, Vaadia E, Bergman H (2001) Activity of pallidal and striatal tonically active neurons is correlated in MPTP-treated monkeys but not in normal monkeys. J Neurosci 21:RC128(1-5).
71. Rubchinsky LL, Kopell N, Sigvardt KA (2003) Modeling facilitation and inhibition of competing motor programs in basal ganglia subthalamic nucleus-pallidal circuits. Proc Natl Acad Sci USA 100:14427-14432.
72. Sandstrom MI, Rebec GV (2003) Characterization of striatal activity in conscious rats: contribution of NMDA and AMPA/kainate receptors to both spontaneous and glutamate-driven firing. Synapse 47:91-100.
73. Schultz W, Apicella P, Ljungberg T (1993) Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J Neurosci 13:900-913.
74. Shriki O, Hansel D, Sompolinsky H (2003) Rate models for conductance-based cortical neuronal networks. Neural Comput 15:1809-1841.
75. Slaght SJ, Paz T, Chavez M, Deniau JM, Mahon S, Charpier S (2004) On the activity of the corticostriatal networks during spike-and-wave discharges in a genetic model of absence epilepsy. J Neurosci 24:6816-6825.
76. Soares J, Kliem MA, Betarbet R, Greenamyre JT, Yamamoto B, Wichmann T (2004) Role of external pallidal segment in primate parkinsonism: comparison of the effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridineinduced parkinsonism and lesions of the external pallidal segment. J Neurosci 24:6417-6426.
77. Strogatz SH (1994) Nonlinear dynamics and chaos: with applications in physics, biology, chemistry, and engineering. Cambridge, MA: Westview. Tepper JM, Koos T, Wilson CJ (2004) GABAergic microcircuits in the neostriatum. Trends Neurosci 27:662-669.
78. Terman D, Rubin J, Yew A, Wilson C (2002) Activity patterns in a model for the subthalamopallidal network of the basal ganglia. J Neurosci 22:2963-2976.
79. Tseng KY, Kasanetz F, Kargieman L, Riquelme LA, Murer MG (2001) Cortical slow oscillatory activity is reflected in the membrane potential and spike trains of striatal neurons in rats with chronic nigrostriatal lesions. J Neurosci 21:6430-6439.
80. Turner RS, Anderson ME (1997) Pallidal discharge related to the kinematics of reaching movements in two dimensions. J Neurophysiol 77:1051-1074.
81. Venance L, Glowinski J, Giaume C (2004) Electrical and chemical transmission between striatal GABAergic output neurones in rat brain slices. J Physiol (Lond) 559:215-230.
82. Wang XJ (2002) Probabilistic decision making by slow reverberation in cortical circuits. Neuron 36:955-968.
83. Wickens JR, Alexander ME, Miller R (1991) Two dynamic modes of striatal function under dopaminergic-cholinergic control: simulation and analysis of a model. Synapse 8:1-12.
84. Wilson HR, Cowan JD (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12:1-24.
85. Wu Y, Richard S, Parent A (2000) The organization of the striatal output system: a single-cell juxtacellular labeling study in the rat. Neurosci Res 38:49-62.