A Persistent Na+ Current and Its Contribution to Burst-Like Firing in Ventral Tegmental Area Dopamine Neurons

Susumu Koyama; Munechika Enjoji; Mark S. Brodie; Sarah B. Appel

doi:10.4236/jbise.2015.87040

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JBiSE> Vol.8 No.7, July 2015

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A Persistent Na⁺ Current and Its Contribution to Burst-Like Firing in Ventral Tegmental Area Dopamine Neurons

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DOI: 10.4236/jbise.2015.87040 2,392 Downloads 2,893 Views Citations

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Susumu Koyama^1,2*, Munechika Enjoji², Mark S. Brodie¹, Sarah B. Appel¹

Affiliation(s)

¹Department of Physiology and Biophysics, University of Illinois at Chicago, College of Medicine, Chicago, IL, USA.
²Department of Clinical Pharmacology, Faculty of Pharmaceutical Sciences, Fukuoka University, Fukuoka, Japan.

ABSTRACT

The ventral tegmental area dopamine (DA VTA) neurons have the spontaneous tonic activity and an alteration of firing pattern from tonic to burst accelerates dopamine transmission more effectively in the mesoaccumbal dopaminergic system, leading to the reinforcing process of drugs of abuse such as alcohol and nicotine. In the present study, we examined whether a persistent Na+ current would contribute to burst firing in DA VTA neuronsusing nystatin-perforated recording. Tetrodotoxin (TTX) (1 μM) or riluzole (10 μM) hyperpolarized the membrane potential and stopped spontaneous firing of DA VTA neurons. In voltage-clamp analysis, a TTX and riluzole-sensitive and persistent Na+ current was activated at ?60 mV and reached maximal amplitude at ?40 mV. This persistent Na+ current was potentiated by a negative shift of the voltage of activation by eliminating Ca²⁺ from the extracellular solution. The Ca²⁺-free extracellular solution depolarized the membrane potential and increased the firing frequency of DA VTA neurons. When a continuous hyperpolarizing current was injected, the firing pattern of the DA VTA neurons transformed into burst-like firing; with average spike number of 4.9, average inter-spike interval of 221 ms, and an average plateau potential, on which the train of spikes generated, was 11 mV. The burst-like firing of DA VTA neurons was abolished by 10 μM riluzole. The concurrent blockade of both T-type Ca²⁺ current and small conductance Ca²⁺-activated K⁺(SK) currents by 100 μM nickel did not induce burst-like firing with or without continuous hyperpolarizing current injection in DA VTA neurons. In conclusion, increases in a persistent Na+ current that mediates a depolarizing driving force by removing extracellular Ca²⁺ contributes to burst-like firing in DA VTA neurons.

KEYWORDS

Apamin, Acutely Dissociated Neurons, Extracellular Ca²⁺, Nickel, Nystatin, Perforated Patch Recording

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Koyama, S. , Enjoji, M. , Brodie, M. and Appel, S. (2015) A Persistent Na⁺ Current and Its Contribution to Burst-Like Firing in Ventral Tegmental Area Dopamine Neurons. Journal of Biomedical Science and Engineering, 8, 429-440. doi: 10.4236/jbise.2015.87040.

References

[1]	Oades, R.D. and Halliday, G.M. (1987) Ventral tegmental (A10) System: Neurobiology. 1. Anatomy and Connectivity. Brain Research, 434, 117-165. http://dx.doi.org/10.1016/0165-0173(87)90011-7

[2]	Appel S.B., McBride, W.J., Diana, M., Diamond, I., Bonci, A. and Brodie, MS. (2004) Ethanol Effects on Dopaminergic “Reward” Neurons in the Ventral Tegmental Area and the Mesolimbic Pathway. Alcoholism: Clinical and Experimental Research, 28, 1768-1778. http://dx.doi.org/10.1097/01.ALC.0000145976.64413.21

[3]	McBride, W.J., Murphy, J.M. and Ikemoto, S. (1999) Localization of Brain Reinforcement Mechanisms: Intracranial Self-Administration and Intracranial Place-Conditioning Studies. Behavioural Brain Research, 101, 129-152. http://dx.doi.org/10.1016/S0166-4328(99)00022-4

[4]	Robinson, T.E. and Berridge, K.C. (2003) Addiction. Annual Review of Psychology, 54, 25-53. http://dx.doi.org/10.1146/annurev.psych.54.101601.145237

[5]	Wise, R.A. (2002) Brain Reward Circuitry: Insights from Unsensed Incentives. Neuron, 36, 229-240. http://dx.doi.org/10.1016/S0896-6273(02)00965-0

[6]	Brodie, M.S., Pesold, C. and Appel, S.B. (1999) Ethanol Directly Excites Dopaminergic Ventral Tegmental Area Reward Neurons. Alcoholism: Clinical and Experimental Research, 11, 1848-1852. http://dx.doi.org/10.1111/j.1530-0277.1999.tb04082.x

[7]	Johnson, S.W. and North, R.A. (1992) Two Types of Neurone in the Rat Ventral Tegmental Area and Their Synaptic Inputs. Journal of Physiology (London), 450, 455-468. http://dx.doi.org/10.1113/jphysiol.1992.sp019136

[8]	Koyama, S. and Appel, S.B. (2006) Characterization of M-Current in Ventral Tegmental Area Dopamine Neurons. Journal of Neurophysiology, 96, 535-544. http://dx.doi.org/10.1152/jn.00574.2005

[9]	Koyama, S., Kanemitsu, Y. and Weight, F.F. (2005) Spontaneous Activity and Properties of Two Types of Principal Neurons from the Ventral Tegmental Area of Rat. Journal of Neurophysiology, 93, 3282-3293. http://dx.doi.org/10.1152/jn.00776.2004

[10]	Neuhoff, H., Neu, A., Liss, B. and Roeper, J. (2002) Ih Channels Contribute to the Different Functional Properties of Identified Dopaminergic Subpopulations in the Midbrain. Journal of Neuroscience, 22, 1290-1302.

[11]	Gonon, F.G. (1988) Nonlinear Relationship between Impulse Flow and Dopamine Released by Rat Midbrain Dopaminergic Neurons as Studied by in Vivo Electrochemistry. Neuroscience, 24, 19-28. http://dx.doi.org/10.1016/0306-4522(88)90307-7

[12]	Chiodo, L.A., Bannon, M.J., Grace, A.A., Roth, R.H. and Bunney, B.S. (1984) Evidence for the Absence of Impulse-Regulating Somatodendritic and Synthesis-Modulating Nerve Terminal Autoreceptors on Subpopulations of Mesocortical Dopamine Neurons. Neuroscience, 12, 1-16. http://dx.doi.org/10.1016/0306-4522(84)90133-7

[13]	Kiyatkin, E.A. and Rebec, G.V. (1998) Heterogeneity of Ventral Tegmental Area Neurons: Single-Unit Recording and Iontophoresis in Awake, Unrestrained Rats. Neuroscience, 85, 1285-1309. http://dx.doi.org/10.1016/S0306-4522(98)00054-2

[14]	Hyland, B.I., Reynolds, J.N., Hay, J., Perk, C.G. and Miller, R. (2002) Firing Modes of Midbrain Dopamine Cells in the Freely Moving Rat. Neuroscience, 114, 475-492. http://dx.doi.org/10.1016/S0306-4522(02)00267-1

[15]	Chergui, K., Suaud-Chagny, M.F. and Gonon, F. (1994) Non-linear Relationship between Impulse Flow, Dopamine Release and Dopamine Elimination in the Rat Brain in Vivo. Neuro-science, 62, 641-645. http://dx.doi.org/10.1016/0306-4522(94)90465-0

[16]	Garris, P.A., Ciolkowski, E.L., Pastore, P. and Wightman, R.M. (1994) Efflux of Dopamine from the Synaptic Cleft in the Nucleus Accumbens of the Rat Brain. Journal of Neuroscience, 14, 6084-6093.

[17]	Grace, A.A. (1987) The Regulation of Dopamine Neuron Activity as Determined by in Vivo and in Vitro Intracellular Recordings. In: Chiodo, L.A. and Freeman, A.S., Eds., Neurophysiology of Dopaminergic Systems—Current Status and Clinical Perspectives, Lakeshore Publishing Company, Detroit, 1-66.

[18]	Grace, A.A. and Bunney, B.S. (1984) The Control of Firing Pattern in Nigral Dopamine Neurons: Burst Firing. Journal of Neuroscience, 4, 2877-2890.

[19]	Carr, D.B. and Sesack, S.R. (2000) Projections from the Rat Prefrontal Cortex to the Ventral Tegmental Area: Target Specificity in the Synaptic Associations with Mesoaccumbens and Mesocortical Neurons. Journal of Neuroscience, 20, 3864-3873.

[20]	Johnson, S.W., Seutin, V. and North, R.A. (1992) Burst Firing in Dopamine Neurons Induced by N-Methyl-D-Aspartate: Role of Electrogenic Sodium Pump. Science, 258, 665-667. http://dx.doi.org/10.1126/science.1329209

[21]	Mereu, G., Lilliu, V., Casula, A., Vargiu, P.F., Diana, M., Musa, A. and Gessa, G.L. (1997) Spontaneous Bursting Activity of Dopaminergic Neurons in Midbrain Slices from Immature Rats: Role of N-Methyl-D-Aspartate Receptors. Neuroscience, 77, 1029-1036. http://dx.doi.org/10.1016/S0306-4522(96)00474-5

[22]	Paladini, C.A., Iribe, Y. and Tepper, J.M. (1999) GABAA Receptor Stimulation Blocks NMDA-Induced Bursting of Dopaminergic Neurons in Vitro by Decreasing Input Resistance. Brain Research, 832, 145-151. http://dx.doi.org/10.1016/S0006-8993(99)01484-5

[23]	Wang, T., O’Connor, W.T., Ungerstedt, U. and French, E.D. (1994) N-Methyl-D-Aspartic Acid Biphasically Regulates the Biochemical and Electrophysiological Response of A10 Dopamine Neurons in the Ventral Tegmental Area: In Vivo Microdialysis and in Vitro Electrophysiological Studies. Brain Research, 666, 255-262. http://dx.doi.org/10.1016/0006-8993(94)90780-3

[24]	Fujimura, K. and Matsuda, Y. (1989) Autogenous Oscillatory Potentials in Neurons of the Guinea Pig Substantia Nigra Pars Compacta in Vitro. Neuroscience Letters, 104, 53-55. http://dx.doi.org/10.1016/0304-3940(89)90328-5

[25]	Kang, Y. and Kitai, S.T. (1993) Calcium Spike Underlying Rhythmic Firing in Dopaminergic Neurons of the Rat Substantia Nigra. Neuroscience Research, 18, 195-207. http://dx.doi.org/10.1016/0168-0102(93)90055-U

[26]	Nedergaard, S., Flatman, J.A. and Engberg, I. (1993) Nifedipine- and ω-Conotoxin-Sensitive Ca2+ Conductances in Guinea-Pig Substantia Nigra Pars Compacta Neurones. Journal of Physiology, 466, 727-747.

[27]	Zhang, L., Liu, Y. and Chen, X. (2005) Carbachol Induces Burst Firing of Dopamine Cells in the Ventral Tegmental Area by Promoting Calcium Entry through L-Type Channels in the Rat. Journal of Physiology, 568, 469-481. http://dx.doi.org/10.1113/jphysiol.2005.094722

[28]	Ping, H.X. and Shepard, P.D. (1996) Apamin-Sensitive Ca2+-Activated K+ Channels Regulate Pacemaker Activity in Nigral Dopamine Neurons. NeuroReport, 7, 809-814. http://dx.doi.org/10.1097/00001756-199602290-00031

[29]	Prisco, S., Natoli, S., Bernardi, G. and Mercuri, N.B. (2002) Group I Metabotropic Glutamate Receptors Activate Burst Firing in Rat Midbrain Dopaminergic Neurons. Neuro-pharmacology, 42, 289-296. http://dx.doi.org/10.1016/S0028-3908(01)00192-7

[30]	Wolfart, J. and Roeper, J. (2002) Selective Coupling of T-Type Calcium Channels to SK Potassium Channels Prevents Intrinsic Bursting in Dopaminergic Midbrain Neurons. Journal of Neuroscience, 22, 3404-3413.

[31]	Agrawal, N., Hamam, B.N., Magistretti, J., Alonso, A. and Ragsdale, D.S. (2001) Persistent Sodium Channel Activity Mediates Subthreshold Membrane Potential Oscillations and Low-Threshold Spikes in Rat Entorhinal Cortex Layer V Neurons. Neuroscience, 102, 53-64. http://dx.doi.org/10.1016/S0306-4522(00)00455-3

[32]	Alonso, A. and Llinas, R.R. (1989) Subthreshold Na+-Dependent Theta-Like Rhythmicity in Stellate Cells of Entorhinal Cortex Layer II. Nature, 342, 175-177. http://dx.doi.org/10.1038/342175a0

[33]	Chapman, C.A. and Lacaille, J.C. (1999) Intrinsic Theta-Frequency Membrane Potential Oscillations in Hippocampal CA1 Interneurons of Stratum Lacunosum-Moleculare. Journal of Neurophysiology, 81, 1296-1307.

[34]	Jinno, S., Ishizuka, S. and Kosaka, T. (2003) Ionic Currents Underlying Rhythmic Bursting of Ventral Mossy Cells in the Developing Mouse Dentate Gyrus. European Journal of Neuroscience, 17, 1338-1354. http://dx.doi.org/10.1046/j.1460-9568.2003.02569.x

[35]	Pape, H.C., Pare, D. and Driesang, R.B. (1998) Two Types of Intrinsic Oscillations in Neurons of the Lateral and Basolateral Nuclei of the Amygdala. Journal of Neuro-physiology, 79, 205-216.

[36]	Bracci, E., Centonze, D., Bernardi, G. and Calabresi, P. (2003) Voltage-Dependent Membrane Potential Oscillations of Rat Striatal Fast-Spiking Interneurons. Journal of Physiology, 549, 121-130. http://dx.doi.org/10.1113/jphysiol.2003.040857

[37]	Boehmer, G., Greffrath, W., Martin, E. and Hermann, S. (2000) Subthreshold Oscillation of the Membrane Potential in Magnocellular Neurones of the Rat Supraoptic Nucleus. Journal of Physiology, 526, 115-128. http://dx.doi.org/10.1111/j.1469-7793.2000.t01-1-00115.x

[38]	Taddese, A. and Bean, B.P. (2001) Subthreshold Sodium Current from Rapidly Inactivating Sodium Channels Drives Spontaneous Firing of Tuberomammillary Neurons. Neuron, 33, 587-600.

[39]	Wu, N., Hsiao, C.F. and Chandler, S.H. (2001) Membrane Resonance and Subthreshold Membrane Oscillations in Mesencephalic V Neurons: Participants in Burst Generation. Journal of Neuroscience, 21, 3729-3739.

[40]	Reboreda, A., Sanchez, E., Romero, M. and Lamas, J.A. (2003) Intrinsic Spontaneous Activity and Subthreshold Oscillations in Neurones of the Rat Dorsal Column Nuclei in Culture. Journal of Physiology, 551, 191-205. http://dx.doi.org/10.1113/jphysiol.2003.039917

[41]	Amir, R., Michaelis, M. and Devor, M. (1999) Membrane Potential Oscillations in Dorsal Root Ganglion Neurons: Role in Normal Electrogenesis and Neuropathic Pain. Journal of Neuroscience, 19, 8589-8596.

[42]	Puopolo, M., Raviola, E. and Bean, B.P. (2007) Roles of Subthreshold Calcium Current and Sodium Current in Spontaneous Firing of Mouse Midbraine Dopamine Neurons. Journal of Neuroscience, 27, 245-656. http://dx.doi.org/10.1523/JNEUROSCI.4341-06.2007

[43]	Astma, N., Gutnick, M.J. and Fleidervish, I.A. (1998) Activation of Protein Kinase C Increases Neuronal Excitability by Regulating Persistent Na+ Current in Mouse Neocortical Slices. Journal of Neurophysiology, 80, 1547-1551.

[44]	Franceschetti, S., Taverna, S., Sancini, G., Panzica, F., Lom-bardi, R. and Avanzini, G. (2000) Protein Kinase C-Dependent Modulation of Na+ Currents Increases the Excitability of Rat Neocortical Pyramidal Neurones. Journal of Physiology, 528, 291-304. http://dx.doi.org/10.1111/j.1469-7793.2000.00291.x

[45]	Pena, F. and Ramirez, J.M. (2002) Endogenous Activation of Serotonin-2A Receptors Is Required for Respiratory Rhythm Generation in Vitro. Journal of Neuroscience, 22, 11055-11064.

[46]	Mantegazza, M., Franceschetti, S. and Avanzini, G. (1998) Anemone Toxin (ATX II)-Induced Increase in Persistent Sodium Current: Effects on the Firing Properties of Rat Neocortical Pyramidal Neurones. Journal of Physiology, 507, 105-116. http://dx.doi.org/10.1111/j.1469-7793.1998.105bu.x

[47]	Shuai, J., Bikson, M., Hahn, P.J., Lian, J. and Durand, D.M. (2003) Ionic Mechanisms Underlying Spontaneous CA1 Neuronal Firing in Ca2+-Free Solution. Biophysical Journal, 84, 2099-2111. http://dx.doi.org/10.1016/S0006-3495(03)75017-6

[48]	Su, H., Alroy, G., Kirson, E.D. and Yaari, Y. (2001) Extracellular Calcium Modulates Persistent Sodium Current-Dependent Burst-Firing in Hippocampal Pyramidal Neurons. Journal of Neuroscience, 21, 4173-4182.

[49]	Neher, E. (1992) Correction for Liquid Junction Potential in Patch Clamp Experiments. Methods in Enzymology, 207, 123-131. http://dx.doi.org/10.1016/0076-6879(92)07008-C

[50]	Brodie, M.S., Shefner, S.A. and Dunwiddie, T.V. (1990) Ethanol Increases the Firing Rate of Dopamine Neurons of the Ventral Tegmental Aria in Vitro. Brain Research, 508, 65-69. http://dx.doi.org/10.1016/0006-8993(90)91118-Z

[51]	Cocatre-Zilgien, J.H. and Delcomyn, F. (1992) Identification of Bursts in Spike Trains. Journal of Neuroscience and Methods, 41, 19-30. http://dx.doi.org/10.1016/0165-0270(92)90120-3

[52]	Kononenko, N.I., Shao, L.R. and Dudek, F.E. (2004) Riluzole-Sensitive Slowly Inactivating Sodium Current in Rat Suprachiasmatic Nucleus Neurons. Journal of Neurophysiology, 91, 710-718. http://dx.doi.org/10.1152/jn.00770.2003

[53]	Urbani, A. and Belluzzi, O. (2000) Riluzole Inhibits the Persistent Sodium Current in Mammalian CNS Neurons. European Journal of Neuroscience, 12, 3567-3574. http://dx.doi.org/10.1046/j.1460-9568.2000.00242.x