Spike frequency adaptation is developmentally regulated in substantia nigra pars compacta dopaminergic neurons

Neuroscience

Volumn 192, Issue , 2011, Pages 1-10

  Vandecasteele, M ^a   Deniau, J M ^a   Venance, L ^a  

^a l'alimentation et l'Environnement   (France)

Author keywords

Dopaminergic neuron; In vitro electrophysiology; Post natal development; SK current; Spike frequency adaptation; Substantia nigra pars compacta

Indexed keywords

APAMIN; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN MATURATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EVOKED RESPONSE; FEMALE; MALE; NERVE CELL STIMULATION; NERVOUS SYSTEM PARAMETERS; NEUROMODULATION; NONHUMAN; PATCH CLAMP; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SPIKE; SPIKE FREQUENCY ADAPTATION; SUBSTANTIA NIGRA PARS COMPACTA;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; DOPAMINERGIC NEURONS; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA;

EID: 80052262462     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.07.017     Document Type: Article

References (61)

1. Allen D., Fakler B., Maylie J., Adelman J.P. Organization and regulation of small conductance Ca2+-activated K+ channel multiprotein complexes. J Neurosci 2007, 27:2369-2376.
2. Arbuthnott G.W., Wickens J. Space, time and dopamine. Trends Neurosci 2007, 30:62-69.
3. Blank T., Nijholt I., Kye M.J., Spiess J. Small conductance Ca2+-activated K+ channels as targets of CNS drug development. Curr Drug Targets CNS Neurol Disord 2004, 3:161-167.
4. Burke R.E. Postnatal developmental programmed cell death in dopamine neurons. Ann N Y Acad Sci 2003, 991:69-79.
5. Chen L.W., Wei L.C., Lang B., Ju G., Chan Y.S. Differential expression of AMPA receptor subunits in dopamine neurons of the rat brain: a double immunocytochemical study. Neuroscience 2001, 106:149-160.
6. Cohen-Matsliah S.I., Motanis H., Rosenblum K., Barkai E. A novel role for protein synthesis in long-term neuronal plasticity: maintaining reduced postburst afterhyperpolarization. J Neurosci 2010, 30:4338-4342.
7. Crook S.M., Ermentrout G.B., Bower J.M. Spike frequency adaptation affects the synchronization properties of networks of cortical oscillators. Neural Comput 1998, 10:837-854.
8. Cui G., Okamoto T., Morikawa H. Spontaneous opening of T-type Ca2+ channels contributes to the irregular firing of dopamine neurons in neonatal rats. J Neurosci 2004, 24:11079-11087.
9. Fallon J.H., Moore R.Y. Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J Comp Neurol 1978, 180:545-580.
10. Floresco S.B., West A.R., Ash B., Moore H., Grace A.A. Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 2003, 6:968-973.
11. Fuhrmann G., Markram H., Tsodyks M. Spike frequency adaptation and neocortical rhythms. J Neurophysiol 2002, 88:761-770.
12. Gargus J.J., Fantino E., Gutman G.A. A piece in the puzzle: an ion channel candidate gene for schizophrenia. Mol Med Today 1998, 4:518-524.
13. Gauthier J., Parent M., Lévesque M., Parent A. The axonal arborization of single nigrostriatal neurons in rats. Brain Res 1999, 834:228-232.
14. Gerfen C.R. The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci 1992, 15:285-320.
15. Gonon F.G. Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry. Neuroscience 1988, 24:19-28.
16. Grace A.A., Bunney B.S. The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 1984, 4:2877-2890.
17. Grace A.A., Bunney B.S. The control of firing pattern in nigral dopamine neurons: single spike firing. J Neurosci 1984, 4:2866-2876.
18. Grace A.A., Onn S.P. Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 1989, 9:3463-3481.
19. Graybiel A.M. Building action repertoires: memory and learning functions of the basal ganglia. Curr Opin Neurobiol 1995, 5:733-741.
20. Graybiel A.M. The basal ganglia: learning new tricks and loving it. Curr Opin Neurobiol 2005, 15:638-644.
21. Grillner P., Mercuri N.B. Intrinsic membrane properties and synaptic inputs regulating the firing activity of the dopamine neurons. Behav Brain Res 2002, 130:149-169.
22. Gu X., Blatz A.L., German D.C. Subtypes of substantia nigra dopaminergic neurons revealed by apamine: autoradiographic and electrophysiological studies. Brain Res Bull 1992, 28:435-440.
23. Hajós M., Greenfield S.A. Topographic heterogeneity of substantia nigra neurons: diversity in intrinsic membrane properties and synaptic inputs. Neuroscience 1993, 55:919-934.
24. Hennequin G., Gerstner W., Pfister J.P. STDP in adaptive neurons gives close-to-optimal information transmission. Front Comput Neurosci 2010, 4:143.
25. Herrik K.F., Christophersen P., Shepard P.D. Pharmacological modulation of the gating properties of small conductance Ca2+-activated K+ channels alters the firing pattern of dopamine neurons in vivo. J Neurophysiol 2010, 104:1726-1735.
26. Hyland B.I., Reynolds J.N., Hay J., Perk C.G., Miller R. Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 2002, 114:475-492.
27. Ji H., Hougaard C., Herrik K.F., Strøbaek D., Christophersen P., Shepard P.D. Tuning the excitability of midbrain dopamine neurons by modulating the Ca2+ sensitivity of SK channels. Eur J Neurosci 2009, 29:1883-1895.
28. Komendantov A.O., Canavier C.C. Electrical coupling between model midbrain dopamine neurons: effects on firing pattern and synchrony. J Neurophysiol 2002, 87:1526-1541.
29. Komendantov A.O., Komendantova O.G., Johnson S.W., Canavier C.C. 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 2004, 91:346-357.
30. Lancaster B., Adams P.R. Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. J Neurophysiol 1986, 55:1268-1282.
31. Liu Y.H., Wang X.J. Spike-frequency adaptation of a generalized leaky integrate-and-fire model neuron. J Comput Neurosci 2001, 10:25-45.
32. Maingret F., Coste B., Hao J., Giamarchi A., Allen D., Crest M., Litchfield D.W., Adelman J.P., Delmas P. Neurotransmitter modulation of small-conductance Ca2+-activated K+ channels by regulation of Ca2+ gating. Neuron 2008, 59:439-449.
33. Mangin J.M., Guyon A., Eugène D., Paupardin-Tritsch D., Legendre P. Functional glycine receptor maturation in the absence of glycinergic input in dopaminergic neurones of the rat substantia nigra. J Physiol 2002, 542:685-697.
34. Mereu G., Lilliu V., Casula A., Vargiu P.F., Diana M., Musa A., Gessa G.L. Spontaneous bursting activity of dopaminergic neurons in midbrain slices from immature rats: role of N-methyl-d-aspartate receptors. Neuroscience 1997, 77:1029-1036.
35. Neuhoff H., Neu A., Liss B., Roeper J. I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 2002, 22:1290-1302.
36. Overton P.G., Clark D. Burst firing in midbrain dopaminergic neurons. Brain Res Brain Res Rev 1997, 25:312-334.
37. Ping H.X., Shepard P.D. Apamine-sensitive Ca(2+)-activated K+ channels regulate pacemaker activity in nigral dopamine neurons. Neuroreport 1996, 7:809-814.
38. Pucak M.L., Grace A.A. Regulation of substantia nigra dopamine neurons. Crit Rev Neurobiol 1994, 9:67-89.
39. Redgrave P., Gurney K. The short-latency dopamine signal: a role in discovering novel actions?. Nat Rev Neurosci 2006, 7:967-975.
40. Reynolds J.N., Wickens J.R. Dopamine-dependent plasticity of corticostriatal synapses. Neural Netw 2002, 15:507-521.
41. Schultz W. Neural coding of basic reward terms of animal learning theory, game theory, microeconomics and behavioural ecology. Curr Opin Neurobiol 2004, 14:139-147.
42. Seroogy K., Ceccatelli S., Schalling M., Hökfelt T., Frey P., Walsh J., Dockray G., Brown J., Buchan A., Goldstein M. A subpopulation of dopaminergic neurons in rat ventral mesencephalon contains both neurotensin and cholecystokinin. Brain Res 1988, 455:88-98.
43. Seutin V., Johnson S.W., North R.A. Apamine increases NMDA-induced burst-firing of rat mesencephalic dopamine neurons. Brain Res 1993, 630:341-344.
44. Seutin V., Massotte L., Renette M.F., Dresse A. Evidence for a modulatory role of Ih on the firing of a subgroup of midbrain dopamine neurons. Neuroreport 2001, 12:255-258.
45. Shepard P.D., Bunney B.S. Effects of apamine on the discharge properties of putative dopamine-containing neurons in vitro. Brain Res 1988, 463:380-384.
46. Sun Q.Q. Experience-dependent intrinsic plasticity in interneurons of barrel cortex layer IV. J Neurophysiol 2009, 102:2955-2973.
47. Tepper J.M., Trent F., Nakamura S. Postnatal development of the electrical activity of rat nigrostriatal dopaminergic neurons. Brain Res Dev Brain Res 1990, 54:21-33.
48. Van Vreeswijk C., Hansel D. Patterns of synchrony in neural networks with spike adaptation. Neural Comput 2001, 13:959-992.
49. Vandecasteele M., Deniau J.-M., Glowinski J., Venance L. Electrical synapses in basal ganglia. Rev Neurosci 2007, 18:15-35.
50. Vandecasteele M., Glowinski J., Deniau J.-M., Venance L. Chemical transmission between dopaminergic neuron pairs. Proc Natl Acad Sci U S A 2008, 105:4904-4909.
51. Vandecasteele M., Glowinski J., Venance L. Electrical synapses between dopaminergic neurons of the substantia nigra pars compacta. J Neurosci 2005, 25:291-298.
52. Vandecasteele M., Glowinski J., Venance L. Connexin mRNA expression in single dopaminergic neurons of substantia nigra pars compacta. Neurosci Res 2006, 56:419-426.
53. Venance L., Glowinski J. Heterogeneity of spike frequency adaptation among medium spiny neurons from the rat striatum. Neuroscience 2003, 122:77-92.
54. Venton B.J., Zhang H., Garris P.A., Phillips P.E., Sulzer D., Wightman R.M. Real-time decoding of dopamine concentration changes in the caudate-putamen during tonic and phasic firing. J Neurochem 2003, 87:1284-1295.
55. Vincent J.B., Paterson A.D., Strong E., Petronis A., Kennedy J.L. The unstable trinucleotide repeat story of major psychosis. Am J Med Genet 2000, 97:77-97.
56. Wang X.J. Calcium coding and adapting temporal computation in cortical pyramidal neurons. J Physiol 1998, 354:319-331.
57. Waroux O., Massotte L., Alleva L., Graulich A., Thomas E., Liégeois J.F., Scuvée-Moreau J., Seutin V. SK channels control the firing pattern of midbrain dopaminergic neurons in vivo. Eur J Neurosci 2005, 22:3111-3121.
58. Wolfart J., Neuhoff H., Franz O., Roeper J. Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J Neurosci 2001, 21:3443-3456.
59. Wolfart J., Roeper J. Selective coupling of T-type calcium channels to SK potassium channels prevents intrinsic bursting in dopaminergic midbrain neurons. J Neurosci 2002, 22:3404-3413.
60. Yin H.H., Knowlton B.J. The role of the basal ganglia in habit formation. Nat Rev Neurosci 2006, 7:464-476.
61. Zhang D., Yang S., Jin G.Z., Bunney B.S., Shi W.X. Oscillatory firing of dopamine neurons: differences between cells in the substantia nigra and ventral tegmental area. Synapse 2008, 62:169-175.