Advertisement

Dopamine pp 243-273 | Cite as

Monitoring Axonal and Somatodendritic Dopamine Release Using Fast-Scan Cyclic Voltammetry in Brain Slices

  • Jyoti C. PatelEmail author
  • Margaret E. Rice
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 964)

Abstract

Brain dopamine pathways serve wide-ranging functions including the control of movement, reward, cognition, learning, and mood. Consequently, dysfunction of dopamine transmission has been implicated in clinical conditions such as Parkinson’s disease, schizophrenia, addiction, and depression. Establishing factors that regulate dopamine release can provide novel insights into dopaminergic communication under normal conditions, as well as in animal models of disease in the brain. Here we describe methods for the study of somatodendritic and axonal dopamine release in brain slice preparations. Topics covered include preparation and calibration of carbon-fiber microelectrodes for use with fast-scan cyclic voltammetry, preparation of midbrain and forebrain slices, and procedures of eliciting and recording electrically evoked dopamine release from in vitro brain slices.

Key words

Dopamine Brain slices Voltammetry Carbon-fiber microelectrodes Striatum Substantia nigra pars compacta Ventral tegmental area 

Notes

Acknowledgments

We are grateful for support from NIH/NINDS grant NS036362 and the Attilio and Olympia Ricciardi Research Fund (M.E.R). We also appreciate critical reading of the manuscript by Melissa A. Stouffer and Harry Xenias.

References

  1. 1.
    Dahlström A, Fuxe K (1964) Evidence of the existence of monoamine-containing neurons in the central nervous system. I: demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol Scand 62:1–55Google Scholar
  2. 2.
    Carlsson A (2002) Treatment of Parkinson’s with L-DOPA. The early discovery phase, and a comment on current problems. J Neural Transm 109:777–787PubMedCrossRefGoogle Scholar
  3. 3.
    Evans AH, Lees AJ (2004) Dopamine dysregulation syndrome in Parkinson’s disease. Curr Opin Neurol 17:393–398PubMedCrossRefGoogle Scholar
  4. 4.
    Cannon CM, Bseikri MR (2004) Is dopamine required for natural reward? Physiol Behav 81:741–748PubMedCrossRefGoogle Scholar
  5. 5.
    Patel JC, Rice ME (2006) Dopamine in brain slices. In: Grimes CA, Dickey EC, Pishko MV (eds) Encyclopedia of sensors, vol 6. American Scientific Publishers, Stevenson Ranch, California, USA, pp 313–334Google Scholar
  6. 6.
    Bull DR, Palij P, Sheehan MJ, Millar J, Stamford JA, Kruk ZL, Humphrey PP (1990) Application of fast cyclic voltammetry to measurement of electrically evoked dopamine overflow from brain slices in vitro. J Neurosci Methods 32:37–44PubMedCrossRefGoogle Scholar
  7. 7.
    Chen BT, Avshalumov MV, Rice ME (2001) H2O2 is a novel, endogenous modulator of synaptic dopamine release. J Neurophysiol 85:2468–2476PubMedGoogle Scholar
  8. 8.
    Patel JC, Witkovsky P, Avshalumov MV, Rice ME (2009) Mobilization of calcium from intracellular stores facilitates somatodendritic dopamine release. J Neurosci 29:6568–6579PubMedCrossRefGoogle Scholar
  9. 9.
    Millar J, Stamford JA, Kruk ZL, Wightman RM (1985) Electrochemical, pharmacological and electrophysiological evidence of rapid dopamine release and removal in the rat caudate nucleus following electrical stimulation of the median forebrain bundle. Eur J Pharmacol 109:341–348PubMedCrossRefGoogle Scholar
  10. 10.
    Patel J, Trout SJ, Kruk ZL (1992) Regional differences in evoked dopamine efflux in brain slices of rat anterior and posterior caudate putamen. Naunyn Schmiedebergs Arch Pharmacol 346:267–276PubMedCrossRefGoogle Scholar
  11. 11.
    Armstrong-James M, Millar J, Kruk ZL (1980) Quantification of noradrenaline iontophoresis. Nature 288:181–183PubMedCrossRefGoogle Scholar
  12. 12.
    Rice ME, Nicholson C (1989) Measurement of nanomolar dopamine diffusion using low-noise perfluorinated ionomer coated carbon fiber microelectrodes and high-speed cyclic voltammetry. Anal Chem 61:1805–1810PubMedCrossRefGoogle Scholar
  13. 13.
    Adams RN (1969) Electrochemistry at solid electrodes. Marcel Dekker, Inc., New York, p 124Google Scholar
  14. 14.
    Millar J, Barnett T (1988) Basic instrumentation for fast cyclic voltammetry. J Neurosci Methods 25:91–95PubMedCrossRefGoogle Scholar
  15. 15.
    Heien ML, Johnson MA, Wightman RM (2004) Resolving neurotransmitters detected by fast-scan cyclic voltammetry. Anal Chem 76:5697–5704PubMedCrossRefGoogle Scholar
  16. 16.
    Armstrong-James M, Millar J (1979) Carbon fibre microelectrodes. J Neurosci Methods 1:279–287PubMedCrossRefGoogle Scholar
  17. 17.
    Kawagoe KT, Zimmerman JB, Wightman RM (1993) Principles of voltammetry and microelectrode surface states. J Neurosci Methods 49:225–240CrossRefGoogle Scholar
  18. 18.
    Cahill PS, Walker QD, Finnegan JM, Mickelson GE, Travis ER, Wightman RM (1996) Microelectrodes for the measurement of catecholamines in biological systems. Anal Chem 68:3180–3186PubMedCrossRefGoogle Scholar
  19. 19.
    Koh DS, Hille B (1999) Rapid fabrication of plastic-insulated carbon-fiber electrodes for micro-amperometry. J Neurosci Methods 88:83–91PubMedCrossRefGoogle Scholar
  20. 20.
    Millar J, Pelling CW (2001) Improved methods for construction of carbon fibre electrodes for extracellular spike recording. J Neurosci Methods 110:1–8PubMedCrossRefGoogle Scholar
  21. 21.
    Gerhardt GA, Hoffman AF (2001) Effects of recording media composition on the responses of Nafion-coated carbon fiber microelectrodes measured using high-speed chronoamperometry. J Neurosci Methods 109:13–21PubMedCrossRefGoogle Scholar
  22. 22.
    Clark JJ, Sandberg SG, Wanat MJ, Gan JO, Horne EA, Hart AS, Akers CA, Parker JG, Willuhn I, Martinez V, Evans SB, Stella N, Phillips PE (2010) Chronic microsensors for longitudinal, subsecond dopamine detection in behaving animals. Nat Methods 7:126–129PubMedCrossRefGoogle Scholar
  23. 23.
    Kume-Kick J, Rice ME (1998) Dependence of dopamine calibration factors on media Ca2+ and Mg2+ at carbon-fiber microelectrodes used with fast-scan cyclic voltammetry. J Neurosci Methods 84:55–62PubMedCrossRefGoogle Scholar
  24. 24.
    Fox K, Armstrong-James M, Millar J (1980) The electrical characteristics of carbon fibre microelectrodes. J Neurosci Methods 3:37–48PubMedCrossRefGoogle Scholar
  25. 25.
    Dingledine R (1984) Brain slices. Plenum Publishing Corporation, New YorkCrossRefGoogle Scholar
  26. 26.
    Rice ME, Richards CD, Nedergaard S, Hounsgaard J, Nicholson C, Greenfield SA (1994) Direct monitoring of dopamine and 5-HT release from substantia nigra and ventral tegmental area in vitro. Exp Brain Res 100:395–406PubMedCrossRefGoogle Scholar
  27. 27.
    MacGregor DG, Chesler M, Rice ME (2001) HEPES prevents edema in rat brain slices. Neurosci Lett 303:141–144PubMedCrossRefGoogle Scholar
  28. 28.
    Avshalumov MV, Patel JC, Rice ME (2008) AMPA receptor-dependent H2O2 generation in striatal medium spiny neurons, but not dopamine axons: one source of a retrograde signal that can inhibit dopamine release. J Neurophysiol 100:1590–1601PubMedCrossRefGoogle Scholar
  29. 29.
    Zhou FM, Liang Y, Dani JA (2001) Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat Neurosci 4:1224–1229PubMedCrossRefGoogle Scholar
  30. 30.
    Sombers LA, Beyene M, Carelli RM, Wightman RM (2009) Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area. J Neurosci 29:1735–1742PubMedCrossRefGoogle Scholar
  31. 31.
    Grace AA, Onn S-P (1989) Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 9:3463–3481PubMedGoogle Scholar
  32. 32.
    Limberger N, Trout SJ, Kruk ZL, Starke K (1991) “Real time” measurement of endogenous dopamine release during short trains of pulses in slices of rat neostriatum and nucleus accumbens: role of autoinhibition. Naunyn Schmiedebergs Arch Pharmacol 344:623–629PubMedCrossRefGoogle Scholar
  33. 33.
    Trout SJ, Kruk ZL (1992) Differences in evoked dopamine efflux in rat caudate putamen, nucleus accumbens and tuberculum olfactorium in the absence of uptake inhibition: influence of autoreceptors. Br J Pharmacol 106:452–458PubMedCrossRefGoogle Scholar
  34. 34.
    Iravani MM, Muscat R, Kruk ZL (1996) Comparison of somatodendritic and axon terminal dopamine release in the ventral tegmental area and the nucleus accumbens. Neuroscience 70:1025–1037PubMedCrossRefGoogle Scholar
  35. 35.
    Rice ME, Cragg SJ, Greenfield SA (1997) Characteristics of electrically evoked somatodendritic dopamine release in substantia nigra and ventral tegmental area in vitro. J Neurophysiol 77:853–862PubMedGoogle Scholar
  36. 36.
    Chen BT, Rice ME (2001) Novel Ca2+ dependence and time course of somatodendritic dopamine release: substantia nigra vs. striatum. J Neurosci 21:7841–7847PubMedGoogle Scholar
  37. 37.
    Elverfors A, Jonason J, Jonason G, Nissbrandt H (1997) Effects of drugs interfering with sodium channels and calcium channels on the release of endogenous dopamine from superfused substantia nigra slices. Synapse 26:359–369PubMedCrossRefGoogle Scholar
  38. 38.
    Iravani MM, Kruk ZL (1995) Effects of amphetamine on carrier-mediated and electrically stimulated dopamine release in slices of rat caudate putamen and nucleus accumbens. J Neurochem 64:1161–1168PubMedCrossRefGoogle Scholar
  39. 39.
    Schmitz Y, Lee CJ, Schmauss C, Gonon F, Sulzer D (2001) Amphetamine distorts stimulation-dependent dopamine overflow: effects on D2 autoreceptors, transporters, and synaptic vesicle stores. J Neurosci 21:5916–5924PubMedGoogle Scholar
  40. 40.
    Patel J, Mooslehner KA, Chan PM, Emson PM, Stamford JA (2003) Presynaptic control of striatal dopamine neurotransmission in adult vesicular monoamine transporter 2 (VMAT2) mutant mice. J Neurochem 85:898–910PubMedCrossRefGoogle Scholar
  41. 41.
    Tecuapetla F, Patel JC, Xenias H, English D, Tadrosi I, Shah F, Berlin J, Deisseroth K, Rice ME, Tepper JM, Koos T (2010) Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens. J Neurosci 30:7105–7110PubMedCrossRefGoogle Scholar
  42. 42.
    Li X, Patel JC, Wang J, Avshalumov MV, Nicholson C, Buxbaum JD, Elder GA, Rice ME, Yue Z (2010) Enhanced striatal dopamine transmission and motor performance with LRRK2 overexpression in mice is eliminated by familial Parkinson’s disease mutation G2019S. J Neurosci 30:1788–1797PubMedCrossRefGoogle Scholar
  43. 43.
    Phillips PEM, Hancock PJ, Stamford JA (2002) Time window of autoreceptor-mediated inhibition of limbic and striatal dopamine release. Synapse 44:15–22PubMedCrossRefGoogle Scholar
  44. 44.
    Chen BT, Moran KA, Avshalumov MV, Rice ME (2006) Limited regulation of somatodendritic dopamine release by voltage-sensitive Ca channels contrasted with strong regulation of axonal dopamine release. J Neurochem 96:645–655PubMedCrossRefGoogle Scholar
  45. 45.
    Rice ME, Cragg SJ (2004) Nicotine amplifies reward-related dopamine signals in striatum. Nat Neurosci 7:583–584PubMedCrossRefGoogle Scholar
  46. 46.
    Bao L, Patel JC, Walker RH, Shashidharan P, Rice ME (2010) Dysregulation of striatal dopamine release in a mouse model of dystonia. J Neurochem 114:1781–1791PubMedCrossRefGoogle Scholar
  47. 47.
    Avshalumov MV, Chen BT, Marshall SP, Peña DM, Rice ME (2003) Glutamate-dependent inhibition of dopamine release in striatum is mediated by a new diffusible messenger, H2O2. J Neurosci 23:2744–2750PubMedGoogle Scholar
  48. 48.
    Voorn P, Vanderschuren LJMJ, Groenewegen HJ, Robbins TR, Pannartz CMA (2004) Putting the spin on the dorsal-ventral divide of the striatum. Trends Neurosci 27:468–474PubMedCrossRefGoogle Scholar
  49. 49.
    Bull DR, Bakhtiar R, Sheehan MJ (1991) Characterization of dopamine autoreceptors in the amygdala: a fast cyclic voltammetric study in vitro. Neurosci Lett 134:41–44PubMedCrossRefGoogle Scholar
  50. 50.
    Jones SR, Garris PA, Kilts CD, Wightman RM (1995) Comparison of dopamine uptake in the basolateral amydaloid nucleus, caudate-putamen, and nucleus accumbens of the rat. J Neurochem 64:2581–2589PubMedCrossRefGoogle Scholar
  51. 51.
    Mundorf ML, Joseph JD, Austin CM, Caron MG, Wightman RM (2001) Catecholamine release and uptake in the mouse prefrontal cortex. J Neurochem 79:130–142PubMedCrossRefGoogle Scholar
  52. 52.
    Cragg SJ, Baufreton J, Xue Y, Bolam JP, Bevan MD (2004) Synaptic release of dopamine in the subthalamic nucleus. Eur J Neurosci 20:1788–1802PubMedCrossRefGoogle Scholar
  53. 53.
    Iravani MM, Kruk ZL (1997) Real-time measurement of stimulated 5-hydroxytryptamine release in rat substantia nigra pars reticulata brain slices. Synapse 25:93–102PubMedCrossRefGoogle Scholar
  54. 54.
    Cragg SJ, Hawkey CR, Greenfield SA (1997) Comparison of serotonin and dopamine release in substantia nigra and ventral tegmental area: region and species differences. J Neurochem 69:2378–2386PubMedCrossRefGoogle Scholar
  55. 55.
    John CE, Budygin EA, Mateo Y, Jones SR (2006) Neurochemical characterization of the release and uptake of dopamine in ventral tegmental area and serotonin in substantia nigra of the mouse. J Neurochem 96:267–282PubMedCrossRefGoogle Scholar
  56. 56.
    Chen BT, Rice ME (2002) Synaptic regulation of somatodendritic dopamine release by glutamate and GABA differs between substantia nigra and ventral tegmental area. J Neurochem 8:158–169CrossRefGoogle Scholar
  57. 57.
    Cragg SJ, Rice ME, Greenfield SA (1997) Heterogeneity of electrically-evoked dopamine release and uptake in substantia nigra, ventral tegmental area, and striatum. J Neurophysiol 77:863–873PubMedGoogle Scholar
  58. 58.
    Jones SR, Mickelson GE, Collins LB, Kawagoe KT, Wightman RM (1994) Interference by pH and Ca2+ ions during measurements of catecholamine release in slices of rat amygdala with fast-scan cyclic voltammetry. J Neurosci Methods 52:1–10PubMedCrossRefGoogle Scholar
  59. 59.
    Wu Q, Reith ME, Wightman RM, Kawagoe KT, Garris PA (2001) Determination of release and uptake parameters from electrically evoked dopamine dynamics measured by real-time voltammetry. J Neurosci Methods 112:119–133PubMedCrossRefGoogle Scholar
  60. 60.
    Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic, IncGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2013

Authors and Affiliations

  1. 1.Departments of Neurosurgery and Physiology & NeuroscienceNew York University School of MedicineNew YorkUSA

Personalised recommendations