Transient high-frequency firing in a coupled-oscillator model of the mesencephalic dopaminergic neuron

Journal of Neurophysiology

Volumn 95, Issue 2, 2006, Pages 932-947

  Kuznetsov, Alexey S ^a,c   Kopell, Nancy J ^a   Wilson, Charles J ^b  

^a Boston University   (United States)

^b UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^c INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CALCIUM; CALCIUM ACTIVATED POTASSIUM CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; POTASSIUM; SODIUM; AMPA RECEPTOR; DOPAMINE;

ANIMAL CELL; ARTICLE; DENDRITIC CELL; DEPOLARIZATION; DOPAMINERGIC NERVE CELL; FREQUENCY MODULATION; HYPERPOLARIZATION; MATHEMATICAL COMPUTING; MESENCEPHALON; NERVE CONDUCTION; NERVE STIMULATION; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; OSCILLATION; OSCILLATORY POTENTIAL; POTASSIUM CURRENT; PRIORITY JOURNAL; SOMATIC CELL; SPIKE WAVE; SYNAPTIC POTENTIAL; ACTION POTENTIAL; ADAPTATION; ANIMAL; BIOLOGICAL MODEL; BIOLOGICAL RHYTHM; COMPUTER SIMULATION; DENDRITE; FEEDBACK SYSTEM; HUMAN; METABOLISM; NERVE CELL; NERVE CELL PLASTICITY; PHYSIOLOGY; SYNAPTIC TRANSMISSION; TIME;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL CLOCKS; COMPUTER SIMULATION; DENDRITES; DOPAMINE; FEEDBACK; HUMANS; MESENCEPHALON; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; NEURONS; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 33644860455     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00691.2004     Document Type: Article

References (70)

1. Albers DS, Weiss SW, Iadarola MJ, and Standaert DG. Immunohistochemical localization of N-methyl-D-aspartate and alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionate receptor subunits in the substantia nigra pars compacta of the rat. Neuroscience 89: 209-220, 1999.
2. Amini B, Clark JW, and Canavier CC. Calcium dynamics underlying pacemaker-like burst firing oscillations in midbrain dopaminergic neurons: a computational study. J Neurophysiol 82: 2249-2261, 1999.
3. Canavier CC. Sodium dynamics underlying burst firing and putative mechanisms for the regulation of the firing pattern in midbrain dopamine neurons: a computational approach. J Comput Neurosci. 6:49-69, 1999.
4. Canavier CC, Perla SR, and Shepard PD. Scaling of prediction error does not confirm chaotic dynamics underlying irregular firing using interspike intervals from midbrain dopamine neurons. Neuroscience 129: 491-502, 2004.
5. Celada P, Paladini CA, and Tepper JM. GABAergic control of rat substantia nigra dopaminergic neurons: role of globus pallidus and substantia nigra pars reticulata. Neuroscience 89: 813-825, 1999.
6. Centonze D, Gubellini P, Pisani A, Bernardi G, and Calabresi P. Dopamine, acetylcholine and nitric oxide systems interact to induce corticostriatal synaptic plasticity. Rev Neurosci 14: 207-216, 2003.
7. Chergui K, Charlety PJ, Akaoka H, Saunier CF, Brunet, J.-L, Buda M, Svensson TH, and Chovet G. Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo. Eur J Neurosci 5:137-144, 1993.
8. Dayan P and Balleine BW. Reward, motivation and reinforcement learning. Neuron 36: 285-298, 2002.
9. Durante P, Cardenas CG, Whittaker JA, Kitai ST, and Scroggs RS. Low-threshold L-type calcium channels in rat dopaminergic neurons. J Neurophysiol 91: 1450-1454, 2004.
10. Ermentrout B. Simulating, Analyzing, and Animating Dynamical Systems: A Guide Toi Xppaut for Researchers and Students. Philadelphia, PA: Society for Industrial and Applied Mathematics, 2002.
11. Fujimura K and Matsuda Y. Autogenous oscillatory potentials in neurons of the guinea pig substantia nigra pars compacta in vitro. Neurosci Lett 104: 53-57, 1989.
12. Grace AA and Bunney BS. Intracellular and extracellular electrophysiology of nigral dopaminergic neurons. I. Identification and characterization. Neuroscience 10: 301-315, 1983a.
13. Grace AA and Bunney BS. Intracellular and extracellular electrophysiology of nigral dopaminergic neurons. II. Action potential generating mechanisms and morphological correlates. Neuroscience 10: 317-331, 1983b.
14. Grace AA and Bunney BS. The control of firing pattern in nigral dopamine neurons: single spike firing. J Neurosci 4: 2866-2876, 1984a.
15. Grace AA and Bunney BS. The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 4: 2877-2890, 1984b.
16. Grace AA and Onn, S.-P. Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 9: 3463-3481, 1989.
17. Grillner P and Mercuri NB. Intrinsic membrane properties and synaptic inputs regulating the firing activity of the dopamine neurons. Behav Brain Res 130:149-169, 2002.
18. Harris NC, Webb C, and Greenfield SA. A possible pacemaker mechanism in pars compacta neurons of the guinea pig substantia nigra revealed by various ion channel blocking agents. Neurosci. 31: 355-362, 1989.
19. Hausser M, Stuart G, Racca C, and Sakmann B. Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron 15: 637-647, 1995.
20. Hyland BI, Reynolds JNJ, Hay J, Perk CG, and Miller R. Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 114: 475-492, 2002.
21. Johnson SW, Seutin V, and North RA. Burst firing in dopamine neurons induced by N-methyl-D-aspartate: role of electrogenic sodium pump. Science 258: 655-657, 1992.
22. Johnson SW and Wu Y-N. Multiple mechanisms underlie burst firing in rat midbrain dopamine neurons in vitro. Brain Res 1019: 293-296, 2004.
23. Juraska JM, Wilson CJ, and Groves PM. The substantia nigra of the rat: a Golgi study. J Comp Neurol 172: 585-600, 1977.
24. Kang Y and Futami T. Arrhythmic firing in dopamine neurons of rat substantia nigra evoked by activation of subthalamic neurons. J Neurophysiol 82: 1632-1637, 1999.
25. Kang Y and Kitai ST. A whole cell patch-clamp study on the pacemaker potential in dopaminergic neurons of rat substantia nigra compacta. Neurosci Res 18: 209-221, 1993a.
26. Kang Y and Kitai ST. Calcium spike underlying rhythmic firing in dopaminergic neurons of the rat substantia nigra. Neurosci Res 18:195-207, 1993b.
27. Kita T, Kita H, and Kitai ST. Electrical membrane properties of rat substantia nigra compacta neurons in an in vitro slice preparation. Brain Res 372: 21-30, 1986.
28. Kitai ST, Shepard PD, Callaway JC, and Scroggs R. Afferent modulation of dopamine neuron firing patterns. Curr Opin Neurobiol 9: 690-697, 1999.
29. Kiyatkin EA and Rebec GV. Heterogeneity of ventral tegmental area neurons: single-unit recording and iontophoresis in awake, unrestrained rats. Neuroscience 85: 1285-1309, 1998.
30. Komendantov AO and Canavier CC. Electrical coupling between model midbrain dopamine neurons: effects on firing pattern and synchrony. J Neurophysiol 87: 1526-1541, 2002.
31. Komendantov AO, Komendantova OG, Johnson SW, and Canavier CC. A modeling study suggests complementary roles for GABAA and NMDA receptors and the SK channel in regulating the firing pattern in midbrain dopamine neurons. J Neurophysiol 91: 346-357, 2004.
32. Kuske R and Erneaux T. Localized synchronization of two coupled solid state lasers. Optical Commun 139: 125-131, 1997.
33. Lacey MG, Mercuri NB, and North RA. Two cell types in rat substantia nigra zona compacta distinguished by membrane properties and the action of dopamine and opoids. J Neurosci 8: 1233-1241, 1987.
34. Li Y-X, Bertram R, and Rinzel J. Modeling N-methyl-D-aspartate-induced bursting in dopamine neurons. Neuroscience 71: 397-410, 1996.
35. Lin JY and Lipski J. Dopaminergic substantia nigra neurons express functional NMDA receptors in postnatal rats. J Neurophysiol 85: 1336-1339, 2001.
36. Lokwan SJA, Overton PG, Berry MS, and Clark D. Stimulation of the pedunculopontine tegmental nucleus in the rat produces burst firing in A9 dopaminergic neurons. Neuroscience 92: 245-254, 1999.
37. Mayer ML and Westbrook GL. The action of N-methyl-D-aspartic acid on mouse spinal neurons in culture. J Physiol 361: 65-90, 1985.
38. Medvedev GS and Kopell N. Synchronization and transient dynamics in chains of electrically coupled FitzHugh-Nagumo oscillations. SIAM J Appl Math 61: 1763-1801, 2001.
39. Medvedev GS, Wilson CJ, Callaway JC, and Kopell N. Dendritic synchrony and transient dynamics in a coupled oscillator model of the dopaminergic neuron. J Comput Neurosci 15: 53-69, 2003.
40. Mercuri NB, Bonci A, Calabresi, P. Stratta F, Stefani A, and Bernardi G. Effects of dihydropyridine calcium antagonists on rat midbrain dopaminergic neurones. Br J Pharmacol 113: 831-838, 1994.
41. 2+ mobilization in dopamine neurons. J Neurosci 23: 149-157, 2003.
42. 2+-independent slow afterhyperpolarization in substantia nigra compacta neurons. Neuroscience 125: 841-852, 2004.
43. 2+ conductances in guinea pig substantia nigra pars compacta neurones. J Physiol 466: 727-747, 1993.
44. Nedergaard S and Greenfield SA. Sub-populations of pars compacta neurons in the substantia nigra: the significance of qualitatively and quantitatively distinct conductances. Neuroscience 48: 423-437, 1992.
45. + spike generation in dendrites of guinea pig substantia nigra pars compacta neurons. Neuroscience 73: 381-396, 1996.
46. Neuhoff H, Neu A, Liss B, and Roeper J. Ih channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 22: 1290-1302, 2002.
47. Nicola SM, Surmeier J, and Malenka RC. Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23: 185-215, 2000.
48. Overton P and Clark D. Iontophoretically administered drugs acting at the N-methyl-D-aspartate receptor modulate burst firing in A9 dopamine neurons in the rat. Synapse 10: 131-140, 1993.
49. Overton PG and Clark D. Burst firing in midbrain dopaminergic neurons. Brain Res Rev 25: 312-334, 1997.
50. B antagonists differentially affect the firing pattern of substantia nigra dopaminergic neurons in vivo. Synapse 32: 165-176, 1999.
51. Paquet M, Tremblay M, Soghomonian JJ, and Smith Y. AMPA and NMDA glutamate receptor subunits in midbrain dopaminergic neurons in the squirrel monkey: an immunohistochemical and in situ hybridization study. J Neurosci 17: 1377-1396, 1997.
52. Paul K, Keith DJ, and Johnson SW. Modulation of calcium-activated potassium small conductance (SK) current in rat dopamine neurons of the ventral tegmental area. Neurosci Lett 2003 348: 180-184, 2003.
53. + channels regulate pacemaker activity in nigral dopamine neurons. Neuroreport 7: 809-814, 1996.
54. Richards CD, Shiroyama T, and Kitai ST. Electrophysiological and immunocytochemical characteristics of GABA and dopamine neurons in the substantia nigra of the rat. Neuroscience 80: 545-557, 1997.
55. Rodriguez M, Pereda E, Gonzalez J, Abdala P, and Obeso JA. How is firing activity of substantia nigra cells regulated? Relevance of pattern-code in the basal ganglia. Synapse 49: 216-225, 2003.
56. Rotstein HG, Kopell N, Zhabotinsky AM, and Epstein IR. A canard mechanism for localization in systems of globally coupled oscillators. SIAM J Appl Math 63: 1998-2019, 2003.
57. Schultz W. Getting formal with dopamine and reward. Neuron 36: 241-263, 2002.
58. Shen K-Z and Johnson SW. Sodium pump evokes high density pump currents in rat midbrain dopamine neurons. J Physiol 512: 449-457, 1998.
59. + conductance. Exp Brain Res 86: 141-150, 1991.
60. Smith ID and Grace AA. Role of the subthalamic nucleus in the regulation of nigral dopamine neuron activity. Synapse 12: 287-303, 1992.
61. Sorenson EM, Shiroyama T, and Kitai ST. Postsynaptic nicotinic receptors on dopaminergic neurons in the substantia nigra pars compacta of the rat. Neuroscience 87: 659-673, 1998.
62. Tepper JM, Martin LP, and Anderson DR. GABAA receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulata projection neurons. J Neurosci 15: 3092-3103, 1995.
63. Tepper JM, Sawyer SF, and Groves PM. Electrophysiologically identified nigral dopaminergic neurons intracellularly labeled with HRP: light-microscopic analysis. J Neurosci 7: 2794-2806, 1987.
64. Tobler PN, Dickinson A, and Schultz W. Coding of predicted reward omission by dopamine neurons in a conditioned inhibition paradigm. J Neurosci 23: 10402-10410, 2003.
65. Tong ZY, Overton PG, and Clark D. Antagonism of NMDA receptors but not AMPA/kainate receptors blocks bursting in dopaminergic neurons induced by stimulation of the prefrontal cortex. J Neural Transm 103: 889-904, 1996.
66. Wilson CJ and Callaway JC. A coupled oscillator model of the dopaminergic neuron of the substantia nigra. J Neurophysiol 83: 3084-3100, 2000.
67. Wilson CJ, Young SJ, and Groves PM. Statistical properties of neuronal spike trains in the substantia nigra: Cell types and their interactions. Brain Res 136: 243-260, 1977.
68. Wolfart J, Neuhoff H, Franz O, and Roeper J. Differential expression of the small-conductance, calcium-activated potassium channel SK2 is critical for pacemaker control in dopaminergic midbrain neurons. J Neurosci 21: 3443-3456, 2001.
69. Wolfart J and Roeper J. Selective coupling of T-type calcium channels to SK potassium channels prevents intrinsic bursting in dopaminergic midbrain neurons. J Neurosci 22: 3404-3413, 2002.
70. Yung WH, Hausser MA, and Jack JJ. Electrophysiology of dopaminergic and non-dopaminergic neurons of the guinea pig substantia nigra pars compacta in vitro. J Physiol 436: 643-667, 1991.