QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

HOME  |   SEARCH  |   ARCHIVE  |   SUBSCRIBE  |   CONTACT  |   HELP

This Article Full Text Full Text (PDF) Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (93) Citing Articles via Google Scholar Google Scholar Articles by Maurice, N. Articles by Surmeier, D. J. Search for Related Content PubMed PubMed Citation Articles by Maurice, N. Articles by Surmeier, D. J.

 Previous Article  |  Next Article 

The Journal of Neuroscience, April 1, 2001, 21(7):2268-2277

D₁/D₅ Dopamine Receptor Activation Differentially Modulates Rapidly Inactivating and Persistent Sodium Currents in Prefrontal Cortex Pyramidal Neurons

Nicolas Maurice¹, Tatiana Tkatch¹, Miriam Meisler², Leslie K. Sprunger², and D. James Surmeier¹

¹ Department of Physiology/Institute for Neuroscience, Northwestern University Medical School, Chicago, Illinois 60611, and ² Department of Human Genetics, University of Michigan, Ann Arbor, Michigan 48109

Dopamine (DA) is a well established modulator of prefrontal cortex (PFC) function, yet the cellular mechanisms by which DA exerts its effects in this region are controversial. A major point of contention is the consequence of D₁ DA receptor activation. Several studies have argued that D₁ receptors enhance the excitability of PFC pyramidal neurons by augmenting voltage-dependent Na⁺ currents, particularly persistent Na⁺ currents. However, this conjecture is based on indirect evidence. To provide a direct test of this hypothesis, we combined voltage-clamp studies of acutely isolated layer V-VI prefrontal pyramidal neurons with single-cell RT-PCR profiling. Contrary to prediction, the activation of D₁ or D₅ DA receptors consistently suppressed rapidly inactivating Na⁺ currents in identified corticostriatal pyramidal neurons. This modulation was attenuated by a D₁/D₅ receptor antagonist, mimicked by a cAMP analog, and blocked by a protein kinase A (PKA) inhibitor. In the same cells the persistent component of the Na⁺ current was unaffected by D₁/D₅ receptor activationsuggesting that rapidly inactivating and persistent Na⁺ currents arise in part from different channels. Single-cell RT-PCR profiling showed that pyramidal neurons coexpressed three -subunit mRNAs (Nav1.1, 1.2, and 1.6) that code for the Na⁺ channel pore. In neurons from Nav1.6 null mice the persistent Na⁺ currents were significantly smaller than in wild-type neurons. Moreover, the residual persistent currents in these mutant neuronswhich are attributable to Nav1.1/1.2 channelswere reduced significantly by PKA activation. These results argue that D₁/D₅ DA receptor activation reduces the rapidly inactivating component of Na⁺ current in PFC pyramidal neurons arising from Nav1.1/1.2 Na⁺ channels but does not modulate effectively the persistent component of the Na⁺ current that is attributable to Nav1.6 Na⁺ channels.

Key words: voltage-clamp; scRT-PCR; neuromodulation; monoamine; Na⁺ channel; molecular biology; protein kinase A; DA receptor; corticostriatal

---

Copyright © 2001 Society for Neuroscience  0270-6474/01/2172268-10$05.00/0

This article has been cited by other articles:

				L. A. Papale, B. Beyer, J. M. Jones, L. M. Sharkey, S. Tufik, M. Epstein, V. A. Letts, M. H. Meisler, W. N. Frankel, and A. Escayg Heterozygous mutations of the voltage-gated sodium channel SCN8A are associated with spike-wave discharges and absence epilepsy in mice Hum. Mol. Genet., May 1, 2009; 18(9): 1633 - 1641. [Abstract] [Full Text] [PDF]

				T. K. Aman, T. M. Grieco-Calub, C. Chen, R. Rusconi, E. A. Slat, L. L. Isom, and I. M. Raman Regulation of Persistent Na Current by Interactions between {beta} Subunits of Voltage-Gated Na Channels J. Neurosci., February 18, 2009; 29(7): 2027 - 2042. [Abstract] [Full Text] [PDF]

				Z. M. Khaliq and B. P. Bean Dynamic, Nonlinear Feedback Regulation of Slow Pacemaking by A-Type Potassium Current in Ventral Tegmental Area Neurons J. Neurosci., October 22, 2008; 28(43): 10905 - 10917. [Abstract] [Full Text] [PDF]

				M. Royeck, M.-T. Horstmann, S. Remy, M. Reitze, Y. Yaari, and H. Beck Role of Axonal NaV1.6 Sodium Channels in Action Potential Initiation of CA1 Pyramidal Neurons J Neurophysiol, October 1, 2008; 100(4): 2361 - 2380. [Abstract] [Full Text] [PDF]

				M. S. Martin, B. Tang, L. A. Papale, F. H. Yu, W. A. Catterall, and A. Escayg The voltage-gated sodium channel Scn8a is a genetic modifier of severe myoclonic epilepsy of infancy Hum. Mol. Genet., December 1, 2007; 16(23): 2892 - 2899. [Abstract] [Full Text] [PDF]

				P. K. Dash, A. N. Moore, N. Kobori, and J. D. Runyan Molecular activity underlying working memory Learn. Mem., August 9, 2007; 14(8): 554 - 563. [Abstract] [Full Text] [PDF]

				S. E. Hammack, I. Mania, and D. G. Rainnie Differential Expression of Intrinsic Membrane Currents in Defined Cell Types of the Anterolateral Bed Nucleus of the Stria Terminalis J Neurophysiol, August 1, 2007; 98(2): 638 - 656. [Abstract] [Full Text] [PDF]

				J. A. Rosenkranz and D. Johnston State-Dependent Modulation of Amygdala Inputs by Dopamine-Induced Enhancement of Sodium Currents in Layer V Entorhinal Cortex J. Neurosci., June 27, 2007; 27(26): 7054 - 7069. [Abstract] [Full Text] [PDF]

				D. C. Rotaru, D. A. Lewis, and G. Gonzalez-Burgos Dopamine D1 receptor activation regulates sodium channel-dependent EPSP amplification in rat prefrontal cortex pyramidal neurons J. Physiol., June 15, 2007; 581(3): 981 - 1000. [Abstract] [Full Text] [PDF]

				D. J. Surmeier Dopamine and working memory mechanisms in prefrontal cortex J. Physiol., June 15, 2007; 581(3): 885 - 885. [Full Text] [PDF]

				E. O. Hernandez-Ochoa, R. E. Garcia-Ferreiro, and D. E. Garcia G protein activation inhibits gating charge movement in rat sympathetic neurons Am J Physiol Cell Physiol, June 1, 2007; 292(6): C2226 - C2238. [Abstract] [Full Text] [PDF]

				T. Ichinose and P. D. Lukasiewicz Ambient Light Regulates Sodium Channel Activity to Dynamically Control Retinal Signaling J. Neurosci., April 25, 2007; 27(17): 4756 - 4764. [Abstract] [Full Text] [PDF]

				W. P. Few, T. Scheuer, and W. A. Catterall Dopamine modulation of neuronal Na+ channels requires binding of A kinase-anchoring protein 15and PKA by a modified leucine zipper motif PNAS, March 20, 2007; 104(12): 5187 - 5192. [Abstract] [Full Text] [PDF]

				L. Chen, J. D. Bohanick, M. Nishihara, J. K. Seamans, and C. R. Yang Dopamine D1/5 Receptor-Mediated Long-Term Potentiation of Intrinsic Excitability in Rat Prefrontal Cortical Neurons: Ca2+-Dependent Intracellular Signaling J Neurophysiol, March 1, 2007; 97(3): 2448 - 2464. [Abstract] [Full Text] [PDF]

				E. Carlier, V. Sourdet, S. Boudkkazi, P. Deglise, N. Ankri, L. Fronzaroli-Molinieres, and D. Debanne Metabotropic glutamate receptor subtype 1 regulates sodium currents in rat neocortical pyramidal neurons J. Physiol., November 15, 2006; 577(1): 141 - 154. [Abstract] [Full Text] [PDF]

				M. P. Abbracchio, G. Burnstock, J.-M. Boeynaems, E. A. Barnard, J. L. Boyer, C. Kennedy, G. E. Knight, M. Fumagalli, C. Gachet, K. A. Jacobson, et al. International Union of Pharmacology LVIII: Update on the P2Y G Protein-Coupled Nucleotide Receptors: From Molecular Mechanisms and Pathophysiology to Therapy Pharmacol. Rev., September 1, 2006; 58(3): 281 - 341. [Abstract] [Full Text] [PDF]

				J. Yagi, H. N. Wenk, L. A. Naves, and E. W. McCleskey Sustained Currents Through ASIC3 Ion Channels at the Modest pH Changes That Occur During Myocardial Ischemia Circ. Res., September 1, 2006; 99(5): 501 - 509. [Abstract] [Full Text] [PDF]

				A. Van Wart and G. Matthews Impaired firing and cell-specific compensation in neurons lacking nav1.6 sodium channels. J. Neurosci., July 5, 2006; 26(27): 7172 - 7180. [Abstract] [Full Text] [PDF]

				M M Trudeau, J C Dalton, J W Day, L P W Ranum, and M H Meisler Heterozygosity for a protein truncation mutation of sodium channel SCN8A in a patient with cerebellar atrophy, ataxia, and mental retardation J. Med. Genet., June 1, 2006; 43(6): 527 - 530. [Abstract] [Full Text] [PDF]

				J. D. Peterson, M. E. Wolf, and F. J. White Repeated amphetamine administration decreases D1 dopamine receptor-mediated inhibition of voltage-gated sodium currents in the prefrontal cortex. J. Neurosci., March 22, 2006; 26(12): 3164 - 3168. [Abstract] [Full Text] [PDF]

				J. A. Rosenkranz and D. Johnston Dopaminergic regulation of neuronal excitability through modulation of Ih in layer V entorhinal cortex. J. Neurosci., March 22, 2006; 26(12): 3229 - 3244. [Abstract] [Full Text] [PDF]

				G. Baranauskas and M. Martina Sodium Currents Activate without a Hodgkin and Huxley-Type Delay in Central Mammalian Neurons J. Neurosci., January 11, 2006; 26(2): 671 - 684. [Abstract] [Full Text] [PDF]

				N. Osorio, G. Alcaraz, F. Padilla, F. Couraud, P. Delmas, and M. Crest Differential targeting and functional specialization of sodium channels in cultured cerebellar granule cells J. Physiol., December 15, 2005; 569(3): 801 - 816. [Abstract] [Full Text] [PDF]

				C. Yue, S. Remy, H. Su, H. Beck, and Y. Yaari Proximal Persistent Na+ Channels Drive Spike Afterdepolarizations and Associated Bursting in Adult CA1 Pyramidal Cells J. Neurosci., October 19, 2005; 25(42): 9704 - 9720. [Abstract] [Full Text] [PDF]

				K. Ptak, G. G. Zummo, G. F. Alheid, T. Tkatch, D. J. Surmeier, and D. R. McCrimmon Sodium Currents in Medullary Neurons Isolated from the Pre-Botzinger Complex Region J. Neurosci., May 25, 2005; 25(21): 5159 - 5170. [Abstract] [Full Text] [PDF]

				N. Wu, A. Enomoto, S. Tanaka, C.-F. Hsiao, D. Q. Nykamp, E. Izhikevich, and S. H. Chandler Persistent Sodium Currents in Mesencephalic V Neurons Participate in Burst Generation and Control of Membrane Excitability J Neurophysiol, May 1, 2005; 93(5): 2710 - 2722. [Abstract] [Full Text] [PDF]

				M. Mantegazza, F. H. Yu, A. J. Powell, J. J. Clare, W. A. Catterall, and T. Scheuer Molecular Determinants for Modulation of Persistent Sodium Current by G-Protein {beta}{gamma} Subunits J. Neurosci., March 30, 2005; 25(13): 3341 - 3349. [Abstract] [Full Text] [PDF]

				Y. Dong, F. J. Nasif, J. J. Tsui, W. Y. Ju, D. C. Cooper, X.-T. Hu, R. C. Malenka, and F. J. White Cocaine-Induced Plasticity of Intrinsic Membrane Properties in Prefrontal Cortex Pyramidal Neurons: Adaptations in Potassium Currents J. Neurosci., January 26, 2005; 25(4): 936 - 940. [Abstract] [Full Text] [PDF]

				Y. Chen, A. R. Cantrell, R. O. Messing, T. Scheuer, and W. A. Catterall Specific Modulation of Na+ Channels in Hippocampal Neurons by Protein Kinase C{epsilon} J. Neurosci., January 12, 2005; 25(2): 507 - 513. [Abstract] [Full Text] [PDF]

				N. Maurice, J. Mercer, C. S. Chan, S. Hernandez-Lopez, J. Held, T. Tkatch, and D. J. Surmeier D2 Dopamine Receptor-Mediated Modulation of Voltage-Dependent Na+ Channels Reduces Autonomous Activity in Striatal Cholinergic Interneurons J. Neurosci., November 17, 2004; 24(46): 10289 - 10301. [Abstract] [Full Text] [PDF]

				Y. Hayashida and A. T. Ishida Dopamine Receptor Activation Can Reduce Voltage-Gated Na+ Current by Modulating Both Entry Into and Recovery From Inactivation J Neurophysiol, November 1, 2004; 92(5): 3134 - 3141. [Abstract] [Full Text] [PDF]

				F. S. Afshari, K. Ptak, Z. M. Khaliq, T. M. Grieco, N. T. Slater, D. R. McCrimmon, and I. M. Raman Resurgent Na Currents in Four Classes of Neurons of the Cerebellum J Neurophysiol, November 1, 2004; 92(5): 2831 - 2843. [Abstract] [Full Text] [PDF]

				M. T. H. Do and B. P. Bean Sodium Currents in Subthalamic Nucleus Neurons From Nav1.6-Null Mice J Neurophysiol, August 1, 2004; 92(2): 726 - 733. [Abstract] [Full Text] [PDF]

				Y. Dong, D. Cooper, F. Nasif, X.-T. Hu, and F. J. White Dopamine Modulates Inwardly Rectifying Potassium Currents in Medial Prefrontal Cortex Pyramidal Neurons J. Neurosci., March 24, 2004; 24(12): 3077 - 3085. [Abstract] [Full Text] [PDF]

				M. J. Craner, B. C. Hains, A. C. Lo, J. A. Black, and S. G. Waxman Co-localization of sodium channel Nav1.6 and the sodium-calcium exchanger at sites of axonal injury in the spinal cord in EAE Brain, February 1, 2004; 127(2): 294 - 303. [Abstract] [Full Text] [PDF]

				J. E. Hanson, Y. Smith, and D. Jaeger Sodium Channels and Dendritic Spike Initiation at Excitatory Synapses in Globus Pallidus Neurons J. Neurosci., January 14, 2004; 24(2): 329 - 340. [Abstract] [Full Text] [PDF]

				T. M. Grieco and I. M. Raman Production of Resurgent Current in NaV1.6-Null Purkinje Neurons by Slowing Sodium Channel Inactivation with {beta}-Pompilidotoxin J. Neurosci., January 7, 2004; 24(1): 35 - 42. [Abstract] [Full Text] [PDF]

				A. T. Gulledge and G. J. Stuart Action Potential Initiation and Propagation in Layer 5 Pyramidal Neurons of the Rat Prefrontal Cortex: Absence of Dopamine Modulation J. Neurosci., December 10, 2003; 23(36): 11363 - 11372. [Abstract] [Full Text] [PDF]

				N. Brunel Dynamics and Plasticity of Stimulus-selective Persistent Activity in Cortical Network Models Cereb Cortex, November 1, 2003; 13(11): 1151 - 1161. [Abstract] [Full Text] [PDF]

				S. Otani, H. Daniel, M.-P. Roisin, and F. Crepel Dopaminergic Modulation of Long-term Synaptic Plasticity in Rat Prefrontal Neurons Cereb Cortex, November 1, 2003; 13(11): 1251 - 1256. [Abstract] [Full Text] [PDF]

				A. J. Gruber, S. A. Solla, D. J. Surmeier, and J. C. Houk Modulation of Striatal Single Units by Expected Reward: A Spiny Neuron Model Displaying Dopamine-Induced Bistability J Neurophysiol, August 1, 2003; 90(2): 1095 - 1114. [Abstract] [Full Text] [PDF]

				Z. M. Khaliq, N. W. Gouwens, and I. M. Raman The Contribution of Resurgent Sodium Current to High-Frequency Firing in Purkinje Neurons: An Experimental and Modeling Study J. Neurosci., June 15, 2003; 23(12): 4899 - 4912. [Abstract] [Full Text] [PDF]

				Y. Dong and F. J. White Dopamine D1-Class Receptors Selectively Modulate a Slowly Inactivating Potassium Current in Rat Medial Prefrontal Cortex Pyramidal Neurons J. Neurosci., April 1, 2003; 23(7): 2686 - 2695. [Abstract] [Full Text] [PDF]

				J. Baufreton, M. Garret, A. Rivera, A. de la Calle, F. Gonon, B. Dufy, B. Bioulac, and A. Taupignon D5 (Not D1) Dopamine Receptors Potentiate Burst-Firing in Neurons of the Subthalamic Nucleus by Modulating an L-Type Calcium Conductance J. Neurosci., February 1, 2003; 23(3): 816 - 825. [Abstract] [Full Text] [PDF]

				J. A. Kearney, D. A. Buchner, G. de Haan, M. Adamska, S. I. Levin, A. R. Furay, R. L. Albin, J. M. Jones, M. Montal, M. J. Stevens, et al. Molecular and pathological effects of a modifier gene on deficiency of the sodium channel Scn8a (Nav1.6) Hum. Mol. Genet., October 15, 2002; 11(22): 2765 - 2775. [Abstract] [Full Text] [PDF]

				D. B. Carr, D. C. Cooper, S. L. Ulrich, N. Spruston, and D. J. Surmeier Serotonin Receptor Activation Inhibits Sodium Current and Dendritic Excitability in Prefrontal Cortex via a Protein Kinase C-Dependent Mechanism J. Neurosci., August 15, 2002; 22(16): 6846 - 6855. [Abstract] [Full Text] [PDF]

				S. Gasparini and J. C Magee Phosphorylation-dependent differences in the activation properties of distal and proximal dendritic Na+ channels in rat CA1 hippocampal neurons J. Physiol., June 15, 2002; 541(3): 665 - 672. [Abstract] [Full Text] [PDF]

				T. M. Grieco, F. S. Afshari, and I. M. Raman A Role for Phosphorylation in the Maintenance of Resurgent Sodium Current in Cerebellar Purkinje Neurons J. Neurosci., April 15, 2002; 22(8): 3100 - 3107. [Abstract] [Full Text] [PDF]

				N. Lezcano and C. Bergson D1/D5 Dopamine Receptors Stimulate Intracellular Calcium Release in Primary Cultures of Neocortical and Hippocampal Neurons J Neurophysiol, April 1, 2002; 87(4): 2167 - 2175. [Abstract] [Full Text] [PDF]

				H. Neuhoff, A. Neu, B. Liss, and J. Roeper Ih Channels Contribute to the Different Functional Properties of Identified Dopaminergic Subpopulations in the Midbrain J. Neurosci., February 15, 2002; 22(4): 1290 - 1302. [Abstract] [Full Text] [PDF]

				G. Gonzalez-Burgos and G. Barrionuevo Voltage-Gated Sodium Channels Shape Subthreshold EPSPs in Layer 5 Pyramidal Neurons From Rat Prefrontal Cortex J Neurophysiol, October 1, 2001; 86(4): 1671 - 1684. [Abstract] [Full Text] [PDF]

Home  |   Search  |   Archive  |   Subscribe  |   Contact  |   Help