Encyclopedia of Computational Neuroscience

Living Edition
| Editors: Dieter Jaeger, Ranu Jung

Basal Ganglia: Dopaminergic Cell Models

  • Alexey KuznetsovEmail author
  • Boris Gutkin
Living reference work entry

Latest version View entry history

DOI: https://doi.org/10.1007/978-1-4614-7320-6_86-3
  • 2 Downloads

Definition

  • Dopaminergic (DA) neurons are defined as neurons synthesizing and containing the neurotransmitter and neurohormone dopamine. Such neurons release dopamine synaptically as well as dendritically (Bustos et al. 2004).

  • The electrophysiological signatures of this neuron are broad action potentials (Fig. 1) and a low-frequency, regular spontaneous activity (Fig. 2a).

  • A distinctive property of the DA neuron is that it differentially responds to different types of excitatory synaptic inputs (Fig. 2a, b).

  • Models have explained these properties and connected them with one another and with particular current compositions (Figs. 3 and 4).

This is a preview of subscription content, log in to check access.

References

  1. Amini B, Clark JW, Canavier CC (1999) Calcium dynamics underlying pacemaker-like burst firing oscillations in midbrain dopaminergic neurons: a computational study. J Neurophysiol 82:2249–2261PubMedCrossRefPubMedCentralGoogle Scholar
  2. Blythe SN, Wokosin D, Atherton JF, Bevan MD (2009) Cellular mechanisms underlying burst firing in substantia nigra dopamine neurons. J Neurosci 49:15531–15541CrossRefGoogle Scholar
  3. Braver TS, Barch DM (2002) A theory of cognitive control, aging cognition, and neuromodulation. Neurosci Biobehav Rev V26(7):809–817.  https://doi.org/10.1016/S0149-7634(02)00067-2CrossRefGoogle Scholar
  4. Bustos G, Abarca J, Campusano J, Bustos V, Noriega V, Aliaga E (2004) Functional interactions between somatodendritic dopamine release, glutamate receptors and brain-derived neurotrophic factor expression in mesencephalic structures of the brain. Brain Res Rev 47(1–3):126–144PubMedCrossRefPubMedCentralGoogle Scholar
  5. Canavier CC (1999) 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 6:49–69PubMedCrossRefPubMedCentralGoogle Scholar
  6. 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 96:2549–2563PubMedPubMedCentralCrossRefGoogle Scholar
  7. Canavier CC, Oprisan S, Callaway J, 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(5):3006–3022PubMedCrossRefPubMedCentralGoogle Scholar
  8. Chan CS, Guzman JN, Ilijic E, Mercer JN, Rick C, Tkatch T, Meredith GE, Surmeier DJ (2007) ‘Rejuvenation’ protects neurons in mouse models of Parkinson’s disease. Nature 447:1081–1086PubMedCrossRefPubMedCentralGoogle Scholar
  9. Chergui K, Charlety PJ, Akaoka H, Saunier CF, Brunet JL, Buda M, Svensson TH, Chovet G (1993) Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo. Eur J Neurosci 5:137–144PubMedCrossRefPubMedCentralGoogle Scholar
  10. Deister CA, Teagarden MA, Wilson CJ, Paladini CA (2009) An intrinsic neuronal oscillator underlies dopaminergic neuron bursting. J Neurosci 50:15888–15897CrossRefGoogle Scholar
  11. Drion G, Massotte L, Sepulchre R, Seutin V (2011) How modeling can reconcile apparently discrepant experimental results: the case of pacemaking in dopaminergic neurons. PLoS Comput Biol 7(5):e1002050PubMedPubMedCentralCrossRefGoogle Scholar
  12. Evans RC, Khaliq ZM (2015) T-type calcium channels trigger a hyperpolarization induced afterdepolarization in substantia nigra dopamine neurons. BMC Neurosci 16:1–2CrossRefGoogle Scholar
  13. Freeman AS, Meltzer LT, Bunney BS (1985) Firing properties of substantia nigra dopaminergic neurons in freely moving rats. Life Sci 36(20):1983–1994PubMedCrossRefPubMedCentralGoogle Scholar
  14. Grace AA, Bunney BS (1984) The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 4:2877–2890PubMedPubMedCentralCrossRefGoogle Scholar
  15. Guzman JN, Sánchez-Padilla J, Chan CS, Surmeier DJ (2009) Robust pacemaking in substantia nigra dopaminergic neurons. J Neurosci 29:11011–11019PubMedPubMedCentralCrossRefGoogle Scholar
  16. Ha J, Kuznetsov A (2011) Frequency switching in a two-compartmental model of the dopaminergic neuron. J Comp Neurosci 30(2):241–254CrossRefGoogle Scholar
  17. Ha J, Kuznetsov A (2013) Interaction of NMDA receptor and pacemaking mechanisms in the midbrain dopaminergic neuron. PLoS One 8(7):e69984PubMedPubMedCentralCrossRefGoogle Scholar
  18. Harris NC, Webb C, Greenfield SA (1989) A possible pacemaker mechanism in pars compacta neurons of the guinea-pig substantia nigra revealed by various ion channel blocking agents. Neuroscience 31:355–362PubMedCrossRefPubMedCentralGoogle Scholar
  19. Hyland BI, Reynolds JNJ, Hay J, Perk CG, Miller R (2002) Firing modes of midbrain dopamine cells in the freely moving rat. J Neurosci 114(2):475–492CrossRefGoogle Scholar
  20. Ji H, Shepard PD (2006) SK Ca2+-activated K+ channel ligands alter the firing pattern of dopamine-containing neurons in vivo. Neuroscience 140(2):623–633PubMedCrossRefPubMedCentralGoogle Scholar
  21. Ji H, Tucker KR, Putzier I, Huertas MA, Horn JP, Canavier CC, Levitan ES, Shepard PD (2012) Functional characterization of ether-à-go-go-related gene potassium channels in midbrain dopamine neurons – implications for a role in depolarization block. Eur J Neurosci 36(7):2906–2916.  https://doi.org/10.1111/j.1460-9568.2012.08190.x
  22. Johnson SW, Wu Y-N (2004) Multiple mechanisms underlie burst firing in rat midbrain dopamine neurons in vitro. Brain Res 1019:293–296PubMedCrossRefPubMedCentralGoogle Scholar
  23. Johnson SW, Seutin V, North RA (1992) Burst firing in dopamine neurons induced by N-methyl-D-aspartate: role of electrogenic sodium pump. Science 258:655–657CrossRefGoogle Scholar
  24. Khaliq ZM, Bean BP (2010) Pacemaking in dopaminergic ventral tegmental area neurons: depolarizing drive from background and voltage-dependent sodium conductances. J Neurosci 30(21):7401–7413PubMedPubMedCentralCrossRefGoogle Scholar
  25. Komendantov AO, Canavier CC (2002) Electrical coupling between model midbrain dopamine neurons: effects on firing pattern and synchrony. J Neurophysiol 87:1526–1541PubMedCrossRefPubMedCentralGoogle Scholar
  26. 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 91:346–357PubMedCrossRefPubMedCentralGoogle Scholar
  27. Kotter R, Feizelmeier M (1998) Species-dependence and relationship of morphological and electrophysiological properties in nigral compacta neurons. Prog Neurobiol 54:619–632PubMedCrossRefPubMedCentralGoogle Scholar
  28. Kuznetsov AS, Kopell NJ, Wilson CJ (2006) Transient high-frequency firing in a coupled-oscillator model of the mesencephalic dopaminergic neuron. J Neurophysiol 95:932–947PubMedCrossRefPubMedCentralGoogle Scholar
  29. Kuznetsova AY, Huertas M, Kuznetsov AS, Papadini C, Canavier C (2010) Regulation of firing frequency in a computational model of a midbrain dopaminergic neuron. J Comp Neuroscience 28(3):389–403CrossRefGoogle Scholar
  30. Li Y-X, Bertram R, Rinzel J (1996) Modeling N-methyl-D-aspartate-induced bursting in dopamine neurons. Neuroscience 71:397–410PubMedCrossRefPubMedCentralGoogle Scholar
  31. Lobb CJ, Wilson CJ, Paladini CA (2010) A dynamic role for GABA receptors on the firing pattern of midbrain dopaminergic neurons. J Neurophysiol 104:403–413PubMedPubMedCentralCrossRefGoogle Scholar
  32. Medvedev GS, Kopell N (2001) Synchronization and transient dynamics in chains of electrically coupled FitzHugh–Nagumo oscillations. SIAM J Appl Math 61:1763–1801CrossRefGoogle Scholar
  33. Medvedev GS, Wilson CJ, Callaway JC, Kopell N (2003) Dendritic synchrony and transient dynamics in a coupled oscillator model of the dopaminergic neuron. J Comput Neurosci 15:53–69PubMedCrossRefGoogle Scholar
  34. Meltzer LT, Christoffersen CL, Serpa KA (1997) Modulation of dopamine neuronal activity by glutamate receptor subtypes. Neurosci Biobehav Rev 21(4):511–518PubMedCrossRefGoogle Scholar
  35. Meza R, López-Jury L, Canavier C, Henny P (2018) Role of the axon initial segment in the control of spontaneous frequency of nigral dopaminergic neurons in vivo. J Neurosci 38(3):733–744PubMedPubMedCentralCrossRefGoogle Scholar
  36. Morikawa H, Khodakhah K, Williams JT (2003) Two intracellular pathways medicate metabotropic glutamate receptor-induced Ca2+ mobilization in dopamine neurons. J Neurosci 23:149–157PubMedPubMedCentralCrossRefGoogle Scholar
  37. Morozova EO, Zakharov D, Gutkin BS, Lapish CC, Kuznetsov A (2016a) Dopamine neurons change the type of excitability in response to stimuli. PLoS Comput Biol 12:e1005233PubMedPubMedCentralCrossRefGoogle Scholar
  38. Morozova EO, Myroshnychenko M, Zakharov D, Di Volo M, Gutkin BS, Lapish CC, Kuznetsov A (2016b) Contribution of synchronized GABAergic neurons to dopaminergic neuron firing and bursting. J Neurophysiol 116:1900–1923PubMedPubMedCentralCrossRefGoogle Scholar
  39. Nedergaard S, Greenfield SA (1992) Sub-populations of pars compacta neurons in the substantia nigra: the significance of qualitatively and quantitatively-distinct conductances. Neuroscience 48:423–437PubMedCrossRefGoogle Scholar
  40. Neuhoff H, Neu A, Liss B, Roeper J (2002) I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 22(4):1290–1302PubMedPubMedCentralCrossRefGoogle Scholar
  41. Oster A, Gutkin BS (2011) A reduced model of DA neuronal dynamics that displays quiescence, tonic firing and bursfing. J Physiol Paris 105(1–3):53–58PubMedCrossRefGoogle Scholar
  42. Overton PG, Clark D (1997) Burst firing in midbrain dopaminergic neurons. Brain Res Rev 25:312–334PubMedCrossRefPubMedCentralGoogle Scholar
  43. Ping HX, Shepard PD (1996) Apamin-sensitive Ca2+-activated K+ channels regulate pacemaker activity in nigral dopamine neurons. Neuroreport 7:809–814PubMedCrossRefPubMedCentralGoogle Scholar
  44. 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 27:645–656PubMedPubMedCentralCrossRefGoogle Scholar
  45. Putzier I, Kullmann PH, Horn JP, Levitan ES (2009) Cav1.3 channel voltage dependence, not Ca2+ selectivity, drives pacemaker activity and amplifies bursts in nigral dopamine neurons. J Neurosci 49:15414–15419CrossRefGoogle Scholar
  46. Qian K, Yu N, Tucker KR, Levitan ES, Canavier CC (2014) Mathematical analysis of depolarization block mediated by slow inactivation of fast sodium channels in midbrain dopamine neurons. J Neurophysiol 112:2779–2790PubMedPubMedCentralCrossRefGoogle Scholar
  47. Redgrave P, Gurney K (2006) The short-latency dopamine signal: a role in discovering novel actions? Nat Rev Neurosci 7(12):967–975PubMedCrossRefPubMedCentralGoogle Scholar
  48. Richards CD, Shiroyama T, Kitai ST (1997) Electrophysiological and immunocytochemical characterization of GABA and dopamine neurons in the substantia nigra of the rat. J Neurosci 80(2):545–557CrossRefGoogle Scholar
  49. Schultz W (2002) Getting formal with dopamine and reward. Neuron 36:241–263PubMedCrossRefPubMedCentralGoogle Scholar
  50. Shepard PD, Bunney BS (1991) Repetitive firing properties of putative dopamine-containing neurons in vitro: regulation by an apamin-sensitive Ca2+-activated K+ conductance. Exp Brain Res 86:141–150PubMedCrossRefPubMedCentralGoogle Scholar
  51. Tepper JM, Martin LP, Anderson DR (1995) GABAA receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulata projection neurons. J Neurosci 15:3092–3103PubMedPubMedCentralCrossRefGoogle Scholar
  52. Tong ZY, Overton PG, Clark D (1996) Antagonism of NMDA receptors but not AMPA/kainate receptors blocks bursting in dopaminergic neurons induced by stimulation of the prefrontal cortex. J Neural Transm 103:889–904PubMedCrossRefGoogle Scholar
  53. Waroux O, Massotte L, Alleva L, Graulich A, Thomas E, Liégeois JF, Scuvée-Moreau J, Seutin V (2005) SK channels control the firing pattern of midbrain dopaminergic neurons in vivo. Eur J Neurosci 22(12):3111–3121PubMedCrossRefPubMedCentralGoogle Scholar
  54. Wilson CJ, Callaway JC (2000) A coupled oscillator model of the dopaminergic neuron of the substantia nigra. J Neurophysiol 83:3084–3100PubMedCrossRefPubMedCentralGoogle Scholar
  55. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483–494PubMedCrossRefPubMedCentralGoogle Scholar
  56. 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(10):3443–3456PubMedPubMedCentralCrossRefGoogle Scholar
  57. Yung WH, Hausser MA, Jack JJ (1991) Electrophysiology of dopaminergic and non-dopaminergic neurons of the guinea-pig substantia nigra pars compacta in vitro. J Physiol (Lond) 436:643–667CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Department of Mathematical SciencesIndiana University and Purdue University IndianapolisIndianapolisUSA
  2. 2.Group for Neural Theory, Laboratoire de Neurosciences Cognitives (LNC), Département d’É tudes CognitivesÉcole Normale SupérieureParisFrance

Section editors and affiliations

  • Jonathan E. Rubin
    • 1
  1. 1.Department of MathematicsUniversity of PittsburghPittsburghUSA