Skip to main content

Burst Firing Induced by N-Methyl-D-Aspartate Requires Activation of an Electrogenic Sodium Pump in Rat Dopamine Neurons

  • Chapter
The Basal Ganglia IV

Part of the book series: Advances in Behavioral Biology ((ABBI,volume 41))

Abstract

In vitro, dopamine neurons in the ventral tegmental area (VTA) and substantia nigra zona compacta (SNC) fire action potentials in a regular pacemaker pattern (Sanghera et al., 1984; Johnson and North, 1992; Grace and Onn, 1989; Lacey et al., 1989). However, in vivo, dopamine neurons fire in bursts (Freeman et al., 1985; Sanghera et al., 1984). The fact that burst firing occurs in vivo but not in vitro implies that afferent connections essential for burst firing are severed in the process of cutting the brain slice (Sanghera et al., 1984). Svensson and Tung (1989) showed that cooling the pre-frontal cortex in the anesthetized rat reversibly blocked burst firing in VTA dopamine neurons. Because prefrontal cortex sends axons which contain excitatory amino acids (EAA’s) to the VTA (Christie et al., 1985), it was thought that cooling the cortex diminished the synaptic release of EAA’s onto dopamine neurons. This conclusion is supported by the findings that glutamate receptor antagonist drugs such kynurenate, 4-(3-phosphonopropyl)-2-piperazine carboxylic acid (CPP), and DL-aminophosphonovaleric acid (APV) reversibly blocked burst firing in dopamine VTA neurons recorded extracellularly in the rat (Charlety et al., 1991; Overton and Clark, 1992; Chergui et al., 1991). In this communication, we report on the mechanism of action underlying burst firing induced by N-methyl-D-aspartate (NMDA) in dopamine neurons in vitro.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Baker, P.F., Blaustein, M.P., Hodgkin, A.L., and Steinhardt, R.A., 1969, The influence of calcium on sodium efflux in squid axons, J. Physiol (Lond.) 200:431–458.

    CAS  Google Scholar 

  • Bean, A.J., and Roth, R.H., 1991, Extracellular dopamine and neurotensin in rat prefrontal cortex in vivo:effects of median forebrain bundle stimulation frequency, stimulation pattern, and dopamine autoreceptors, J. Neurosci. 11:2694–2702.

    PubMed  CAS  Google Scholar 

  • Bissette, G., and Nemeroff, C.B., 1988, Neurotensin and the mesocorticolimbic dopamine system, Ann. N.Y. Acad. Sci. 537:397–404.

    Article  PubMed  CAS  Google Scholar 

  • Blatz, A., and Magleby, K.L., 1986, Single apamin-blocked Ca2+-activated K+ channels of small conductance in cultured rat skeletal muscle, Nature 323:718–720.

    Article  PubMed  CAS  Google Scholar 

  • Charlety, P.J., Grenhoff, J., Chergui, K., De La Chapelle, B., Buda, M., Svensson, T.H., and Chouvet, G., 1991, Burst firing of mesencephalic dopamine neurons is inhibited by somatodendritic application of kynurenate, Acta Physiol. Scand. 142:105–112.

    Article  PubMed  CAS  Google Scholar 

  • Chergui, K., Charlety, P.J., Akaoka, H., Brunet, J.L., Saunier, C.F., Buda, M., Svensson, T.H., and Chouvet, G., 1991, NMDA receptors are involved in spontaneous burst firing of dopaminergic mesencephalic neurons, C.R. Acad. Sci. (Paris) 313:139.

    CAS  Google Scholar 

  • Choi, D.W., 1988, Glutamate neurotoxicity and diseases of the nervous system, Neuron 1:623–634.

    Article  PubMed  CAS  Google Scholar 

  • Christie, M.J., Bridge, S., James, L.B., and Beart, P.M., 1985, Excitotoxin lesions suggest an aspartatergic projection from rat medial prefrontal cortex to ventral tegmental area, Brain Res. 333:169–172.

    Article  PubMed  CAS  Google Scholar 

  • Crawley, J.N., 1991, Cholecystokinin-dopamine interactions, Trend. Pharmacol. Sci. 12:232–236.

    Article  Google Scholar 

  • Creese, I., Burt, D.R., and Snyder, S.H., 1976, Dopamine receptor binding predicts clinical and pharmacological potencies of antischizophrenic drugs, Science 192:481–483.

    Article  PubMed  CAS  Google Scholar 

  • DeLong, M.R., Crutcher, M.D., and Georgopoulos, A.P., 1983, Relations between movement and single cell discharge in the substantia nigra of the behaving monkey, J. Neurosci. 3:1599–1606.

    PubMed  CAS  Google Scholar 

  • Dutton, A., and Dyball, R.E.J., 1979, Phasic firing enhances vasopressin release from the rat neurohypophysis, J. Physiol. (Lond.) 290:433–440.

    CAS  Google Scholar 

  • Freeman, A.S., Meitzer, L.T., and Bunney, B.S., 1985, Firing properties of substantia nigra dopaminergic neurons in freely moving rats, Life Sci. 36:1983–1994.

    Article  PubMed  CAS  Google Scholar 

  • Fukuda, A., and Prince, D.A., 1992, Excessive intracellular Ca2+ inhibits glutamate-induced Na+-K+ pump activation in rat hippocampal neurons, J. Neurophysiol. 68:28–35.

    PubMed  CAS  Google Scholar 

  • Gonon, F.G., 1988, Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry, Neurosci. 24:19–28.

    Article  CAS  Google Scholar 

  • Gonon, F.G., and Buda, M.J., 1985, Regulation of dopamine release by impulse flow and by autoreceptors as studied by in vivo voltammetry in the rat striatum, Neurosci. 14:765–774.

    Article  CAS  Google Scholar 

  • Grace, A.A., 1991, Phasic versus tonic dopamine release and the modulation of dopamine system responsivity:a hypothesis for the etiology of schizophrenia, Neurosci. 41:1–24.

    Article  CAS  Google Scholar 

  • Grace, A.A., and Bunney, B.S., 1984, The control of firing pattern in nigral dopamine neurons:burst firing, J. Neurosci. 4:2877–2890.

    PubMed  CAS  Google Scholar 

  • Grace, A.A., and Onn, S.-P., 1989, Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro, J. Neurosci. 9:3463–3481.

    PubMed  CAS  Google Scholar 

  • Greenamyre, J.T., and O’Brien, C.F., 1991, N-methyl-D-aspartate antagonists in the treatment of Parkinson’s disease, Arch. Neurol. 48:977–981.

    PubMed  CAS  Google Scholar 

  • Hokfelt, T., Everitt, B.H., Thedorsson-Norheim, E., and Goldstein, M., 1984, Occurrence of neurotensin-like immunoreactivity in subpopulations of hypothalamic, mesencephalic and medullary catecholamine neurons, J. Comp. Neurol. 222:543–560.

    Article  PubMed  CAS  Google Scholar 

  • Hokfelt, T., Rehfeld, J.F., Skirboll, L., Ivemark, B., Goldstein, M., and Markey, K., 1980, Evidence for coexistence of dopamine and CCK in mesolimbic neurons, Nature 285:476–478.

    Article  PubMed  CAS  Google Scholar 

  • Hu, B., and Bourque, C.W., 1992, NMDA receptor-mediated rhythmic bursting activity in rat supraoptic nucleus neurones in vitro, J. Physiol. (Lond.)458:667–687.

    CAS  Google Scholar 

  • Jahnsen, H., and Llinas, R., 1984, Ionic basis for the electroresponsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro, J. Physiol. (Lond.) 349:227–247.

    CAS  Google Scholar 

  • Johnson, S.W., North, R.A., 1992, Two types of neurone in the rat ventral tegmental area and their synaptic inputs, J. Physiol. (Lond.) 450:491–502.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Lacey, M.G., Mercuri, N.B., and North, R.A., 1988, On the potassium conductance increase activated by GABA-B and dopamine D-2 receptors in rat substantia nigra neurones, J. Physiol. (Lond.) 401:437–453.

    CAS  Google Scholar 

  • Lacey, M.G., Mercuri, N.B., and North, R.A., 1989, Two cell types in rat substantia nigra zona compacta distinguished by membrane properties and the actions of dopamine and opioids, J. Neurosci. 9:1233–1241.

    PubMed  CAS  Google Scholar 

  • Lancaster, B., and Nicoli, R.A., 1987, Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones, J. Physiol. (Lond.) 389:187–203.

    CAS  Google Scholar 

  • Lees, G.J., 1991, Inhibition of sodium-potassium-ATPase:a potentially ubiquitous mechanism contributing to central nervous system neuropathology, Brain Res. Rev. 16:283–300.

    Article  PubMed  CAS  Google Scholar 

  • Llinas, R., Greenfield, S.A, and Jahnsen, H., 1984, Electrophysiology of pars compacta cells in the in vitro substantia nigra — a possible mechanism for dendritic release, Brain Res. 294:127–132.

    Article  PubMed  CAS  Google Scholar 

  • Mayer, M.L., Westbrook, G L.,1987, Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurones, J. Physiol. (Lond.) 394:501-527.

    CAS  Google Scholar 

  • McCormick, D.A., and Pape, H.-C., 1990, Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones, J. Physiol. (Lond.) 431:291–318.

    CAS  Google Scholar 

  • Miller, C., Moczydlowski, E., Latorre, R., and Phillips, M., 1985, Charybdotoxin, a protein inhibitor of single Ca2+-activated K+ channels from mammalian skeletal muscle, Nature 313:316–318.

    Article  PubMed  CAS  Google Scholar 

  • Miller, J.D., Sanghera, M.K., and German, D.C., 1981, Mesencephalic dopaminergic unit activity in the behaviorally conditioned rat, Life Sci. 29:1255–1263.

    Article  PubMed  CAS  Google Scholar 

  • Overton, P., and Clark, D., 1992, Iontophoretically administered drugs acting at the N-methyl-D-aspartate receptor modulate burst firing in A9 dopamine neurons in the rat, Synapse 10:131–140.

    Article  PubMed  CAS  Google Scholar 

  • Parker, W.D., Boyson, S.J., and Parks, J.K., 1989, Abnormalities of the electron transport chain in idiopathic Parkinson’s disease, Ann. Neurol. 26:719–723.

    Article  PubMed  Google Scholar 

  • Paxinos, G., Watson, C.,1986, “The Rat Brain in Stereotaxic Coordinates,” Second edition, Academic Press Inc., San Diego.

    Google Scholar 

  • Romo, R., and Schultz, W., 1990, Dopamine neurons of the monkey midbrain:contingencies of responses to active touch during self-initiated arm movements, J. Neurophysiol. 63:592–606.

    PubMed  CAS  Google Scholar 

  • Sanghera, M.K., Trulson, M.E., and German, D.C., 1984, Electrophysiological properties of mouse dopamine neurons:in vivo and in vitro studies, Neurosci. 12:793–801.

    Article  CAS  Google Scholar 

  • Schapira, A.H.V., Cooper, J.M., Dexter, D., Clark, J.B., Jenner, P., and Marsden, CD., 1990, Mitochondrial complex I deficiency in Parkinson’s disease, J. Neurochem. 54:823–827.

    Article  PubMed  CAS  Google Scholar 

  • Schultz, W., and Romo, R., 1990, Dopamine neurons of the monkey midbrain:contingencies of responses to stimuli eliciting immediate behavioral reactions, J. Neurophysiol. 63:607–624.

    PubMed  CAS  Google Scholar 

  • Seeman, P., and Lee, T., 1975, Antipsychotic drugs:direct correlation between clinical potency and presynaptic action of dopamine neurons, Science 188:1217–1219.

    Article  PubMed  CAS  Google Scholar 

  • Shepard, P.D., and Bunney, B.S., 1991, Repetitive firing properties of putative dopamine-containing neurons in vitro:regulation by an apamin-sensitive Ca+-activated K+ conductance, Exp. Brain Res. 86:141–150.

    Article  PubMed  CAS  Google Scholar 

  • Silva, N.L., Pechura, CM., and Barker, J.L., 1990, Postnatal rat nigrostriatal dopaminergic neurons exhibit five types of potassium conductances, J. Neurophysiol. 64:262–272.

    PubMed  CAS  Google Scholar 

  • Sonsalla, P.K., Nicklas, W.J., and Heikkila, R.E., 1989, Role for excitatory amino acids in methamphetamine-induced nigrostriatal dopaminergic toxicity, Science 243:398–400.

    Article  PubMed  CAS  Google Scholar 

  • Stys, P.K., Ransom, B.R., Waxman, S.G., and Davis, P.K., 1990, Role of extracellular calcium in anoxic injury of mammalian central white matter, Proc. Natl. Acad. Sci. (USA) 87:4212–4216.

    Article  CAS  Google Scholar 

  • Svensson, T.H., and Tung, C.-S., 1989, Local cooling of pre-frontal cortex induces pacemaker-like firing of dopamine neurons in rat ventral tegmental area in vivo, Acta Physiol. Scand. 136:135–136.

    Article  PubMed  CAS  Google Scholar 

  • Turski, L., Bressler, K., Rettig, K.-J., Loschmann, P.-A., and Wachtel, H., 1991, Protection of substantia nigra from MPP+ neurotoxicity by N-methyl-D-aspartate antagonists, Nature 349:414–418.

    Article  PubMed  CAS  Google Scholar 

  • Willis, J.A., Gaubatz, G.L., and Carpenter, D.O., 1974, The role of the electrogenic sodium pump in modulation of pacemaker discharge of aplysia neurons, J. Cell Physiol. 84:463–472.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1994 Plenum Press, New York

About this chapter

Cite this chapter

Johnson, S.W., Seutin, V., North, R.A. (1994). Burst Firing Induced by N-Methyl-D-Aspartate Requires Activation of an Electrogenic Sodium Pump in Rat Dopamine Neurons. In: Percheron, G., McKenzie, J.S., Féger, J. (eds) The Basal Ganglia IV. Advances in Behavioral Biology, vol 41. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-0485-2_27

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-0485-2_27

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-7591-6

  • Online ISBN: 978-1-4613-0485-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics