How modeling can reconcile apparently discrepant experimental results: The case of pacemaking in dopaminergic neurons

PLoS Computational Biology

Volumn 7, Issue 5, 2011, Pages

  Drion, Guillaume ^a   Massotte, Laurent ^a   Sepulchre, Rodolphe ^a   Seutin, Vincent ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; SODIUM;

DETAILED MODELS; DOPAMINERGIC NEURONS; EXPERIMENTAL PROTOCOLS; L-TYPE CALCIUM CHANNELS; MIDBRAIN; MINIMAL MODEL; POTENTIAL RECORDING; PROPERTY; SODIUM CHANNEL; STATE OF THE ART;

NEURONS;

CALCIUM CHANNEL L TYPE; CALCIUM ION; SODIUM CHANNEL; CALCIUM CHANNEL; DOPAMINE; DOPAMINE RECEPTOR STIMULATING AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CHANNEL GATING; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; MALE; MATHEMATICAL ANALYSIS; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; OSCILLATORY POTENTIAL; RAT; SODIUM CONDUCTANCE; SODIUM CURRENT; SPIKE WAVE; SYNAPTIC TRANSMISSION; ACTION POTENTIAL; ANALYSIS OF VARIANCE; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; CYTOLOGY; DRUG EFFECT; MESENCEPHALON; NERVE CELL; PHYSIOLOGY; WISTAR RAT;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; CALCIUM CHANNELS; COMPUTATIONAL BIOLOGY; DOPAMINE; DOPAMINE AGENTS; MALE; MESENCEPHALON; MODELS, BIOLOGICAL; NEURONS; RATS; RATS, WISTAR; SODIUM CHANNELS;

EID: 79958104418     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002050     Document Type: Article

References (32)

1. Jin X, Costa RM, (2010) Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 466: 457-462.
2. Schultz W, (2007) Behavioral dopamine signals. Trends Neurosci 30: 203-210.
3. Iversen SD, Iversen LL, (2007) Dopamine: 50 years in perspective. Trends Neurosci 30: 188-193.
4. Grace AA, Bunney BS, (1984) The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 4: 2877-2890.
5. Brazhnik E, Shah F, Tepper JM, (2008) GABAergic afferents activate both GABAA and GABAB receptors in mouse substantia nigra dopaminergic neurons in vivo. J Neurosci 28: 10386-10398.
6. Puopolo M, Raviola E, Bean BP, (2007) Roles of subthreshold calcium current and sodium current in spontaneous firing of mouse midbrain dopamine neurons. J Neurosci 27: 645-656.
7. Khaliq ZM, Bean BP, (2010) Pacemaking in dopaminergic ventral tegmental area neurons: depolarizing drive from background and voltage-dependent sodium conductance. J Neurosci 30: 7401-7413.
8. Nedergaard S, Flatman JA, Engberg I, (1993) Nifedipine- and omega-conotoxin-sensitive Ca2+ conductances in guinea-pig substantia nigra pars compacta neurones. J Physiol 466: 727-747.
9. Ping HX, Shepard PD, (1996) Apamin-sensitive Ca2+-activated K+ channels regulate pacemaker activity in nigral dopamine neurons. Neuroreport 7: 809-814.
10. Guzman JN, Sanchez-Padilla J, Chan CS, Surmeier DJ, (2009) Robust pacemaking in substantia nigra dopaminergic neurons. J Neurosci 29: 11011-11019.
11. Putzier I, Kullmann PHM, Horn JP, Levitan ES, (2009) Cav1.3 channel voltage dependence, not Ca(2+) selectivity, drives pacemaker activity and amplifies bursts in nigral dopamine neurons. J Neurosci 29: 15414-15419.
12. Waroux O, Massotte L, Alleva L, Graulich A, Thomas E, et al. (2005) SK channel control the firing pattern of midbrain dopaminergic neurons in vivo. Eur J Neurosci 22: 3111-3121.
13. Ji H, Hougaard C, Herrik KF, Strøbaek D, Christophersen P, et al. (2009) Tuning the excitability of midbrain dopamine neurons by modulating the Ca2+ sensitivity of SK channels. Eur J Neurosci 29: 1883-1895.
14. Canavier CC, Landry RS, (2006) An increase in AMPA and a decrease in SK conductance increase burst firing by different mechanisms in a model of a dopamine neuron in vivo. J Neurophysiol 96: 2549-2563.
15. Drion G, Bonjean M, Waroux O, Scuvée-Moreau J, Liégeois JF, et al. (2010) M-type channels selectively control bursting in rat dopaminergic neurons. Eur J Neurosci 31: 827-835.
16. Hille, B, (2001) Ion Channels of Excitable Membranes. Sunderland (Massachusetts) Sinauer pp. 95-129.
17. Xu W, Lipscombe D, (2001) Neuronal Ca(V)1.3alpha(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci 21: 5944-5951.
18. Izhikevich EM, (2007) Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting. Cambridge (Massachusetts) The MIT Press pp. 325-378.
19. Wolfart J, Neuhoff H, Franz O, Roeper J, (2001) Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J Neurosci 21: 3443-3456.
20. Seutin V, Johnson SW, North RA, (1993) Apamin increases NMDA-induced burst-firing of rat mesencephalic dopamine neurons. Brain Res 630: 341-4.
21. Salvador JM, Inesi G, Rigaud JL, Mata AM, (1998) Ca2+ transport by reconstituted synaptosomal ATPase is associated with H+ countertransport and net charge displacement. J Biol Chem 273: 18230-18234.
22. Seutin V, Engel D, (2010) Differences in Na+ conductance density and Na+ channel functional properties between dopamine and GABA neurons of the rat substantia nigra. J Neurophysiol 103: 3099-30114.
23. Blythe SN, Wokosin D, Atherton JF, Bevan MD, (2009) Cellular mechanisms underlying burst firing in substantia nigra dopamine neurons. J Neurosci 29: 15531-15541.
24. Li YX, Bertram R, Rinzel J, (1996) Modeling N-methyl-D-aspartate-induced bursting in dopamine neurons. Neuroscience 71: 397-410.
25. Amini B, Clark JW Jr, Canavier CC, (1999) Calcium dynamics underlying pacemaker-like and burst firing oscillations in midbrain dopaminergic neurons: a computational study. J Neurophysiol 82: 2249-2261.
26. Wilson CJ, Callaway JC, (2000) Coupled oscillator model of the dopaminergic neuron of the substantia nigra. J Neurophysiol 83: 3084-3100.
27. Komendantov AO, Komendantova OG, Johnson SW, Canavier CC, (2004) 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.
28. Kuznetsov AS, Kopell NJ, Wilson CJ, (2006) Transient high-frequency firing in a coupled-oscillator model of the mesencephalic dopaminergic neuron. J Neurophysiol 95: 932-947.
29. Canavier CC, Oprisan SA, Callaway JC, Ji H, Shepard PD, (2007) Computational model predicts a role for ERG current in repolarizing plateau potentials in dopamine neurons: implications for modulation of neuronal activity. J Neurophysiol 98: 3006-3022.
30. Chan CS, Guzman JN, Ilijic E, Mercer JN, Rick C, et al. (2007) 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature 447: 1081-1086.
31. Hodgkin AL, Huxley AF, (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 177: 500-544.
32. Seutin V, Scuve-Moreau J, Giesbers I, Massotte L, Dresse A, (1990) Effect of BHT 920 on monoaminergic neurons of the rat brain: an electrophysiological in vivo and in vitro study. Naunyn Schmiedebergs Arch Pharmacol 342: 502-507.