In vivo comparison of norepinephrine and dopamine release in rat brain by simultaneous measurements with fast-scan cyclic voltammetry

Journal of Neurochemistry

Volumn 119, Issue 5, 2011, Pages 932-944

  Park, Jinwoo ^a   Takmakov, Pavel ^a   Wightman, R Mark ^a,b  

^a University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

dopamine; fast scan cyclic voltammetry; norepinephrine; nucleus accumbens; ventral bed nucleus of the stria terminalis

Indexed keywords

AMPHETAMINE; DOPAMINE; DOPAMINE AUTORECEPTOR ANTAGONIST; DOPAMINE RECEPTOR BLOCKING AGENT; METIROSINE; NORADRENALIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANTERIOR NUCLEUS ACCUMBENS; ARTICLE; CARBON FIBER MICROELECTRODE; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; ELECTROSTIMULATION; FAST SCAN CYCLIC VOLTAMMETRY; IN VIVO STUDY; MALE; MEASUREMENT; MICROELECTRODE; NONHUMAN; NORADRENALIN RELEASE; NORADRENERGIC NERVE; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; STRIA TERMINALIS; SUBSTANTIA NIGRA; VENTRAL BED NUCLEUS OF STRIA TERMINALIS; VENTRAL TEGMENTUM;

ANIMALS; BIOSENSING TECHNIQUES; DOPAMINE; ELECTRIC STIMULATION; ELECTROCHEMICAL TECHNIQUES; MALE; NOREPINEPHRINE; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; SEPTAL NUCLEI;

ANIMALIA; RATTUS;

EID: 81255135822     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07494.x     Document Type: Article

References (76)

1. Albert G. C., Cook C. M., Prato F. S., and, Thomas A. W., (2009) Deep brain stimulation, vagal nerve stimulation and transcranial stimulation: An overview of stimulation parameters and neurotransmitter release. Neurosci. Biobehav. Rev. 33, 1042-1060.
2. Aragona B. J., Cleaveland N. A., Stuber G. D., Day J. J., Carelli R. M., and, Wightman R. M., (2008) Preferential enhancement of dopamine transmission within the nucleus accumbens shell by cocaine is attributable to a direct increase in phasic dopamine release events. J. Neurosci. 28, 8821-8831.
3. Aston-Jones G., and, Cohen J. D., (2005) An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annu. Rev. Neurosci. 28, 403-450. (Pubitemid 41098911)
4. Aston-Jones G., Segal M., and, Bloom F. E., (1980) Brain aminergic axons exhibit marked variability in conduction velocity. Brain Res. 195, 215-222. (Pubitemid 10077844)
5. Aston-Jones G., Delfs J. M., Druhan J., and, Zhu Y., (1999) The bed nucleus of the stria terminalis-a target site for noradrenergic actions in opiate withdrawal. Advancing from the Ventral Striatum to the Extended Amygdala 877, 486-498. (Pubitemid 29351874)
6. Baur J. E., Kristensen E. W., May L. J., Wiedemann D. J., and, Wightman R. M., (1988) Fast-scan voltammetry of biogenic-amines. Anal. Chem. 60, 1268-1272.
7. Berridge C. W., and, Waterhouse B. D., (2003) The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res. Rev. 42, 33-84. (Pubitemid 36369264)
8. Burmeister J. J., Pomerleau F., Palmer M., Day B. K., Huettl P., and, Gerhardt G. A., (2002) Improved ceramic-based multisite microelectrode for rapid measurements of L-glutamate in the CNS. J. Neurosci. Methods 119, 163-171. (Pubitemid 35286982)
9. Cahill P. S., and, Wightman R. M., (1995) Simultaneous amperometric measurement of ascorbate and catecholamine secretion from individual bovine adrenal-medullary cells. Anal. Chem. 67, 2599-2605.
10. Capella P., Ghasemzadeh M. B., Adams R. N., Wiedemann D. J., and, Wightman R. M., (1993) Real-time monitoring of electrically stimulated norepinephrine release in rat thalamus. 2. Modeling of release and reuptake characteristics of stimulated norepinephrine overflow. J. Neurochem. 60, 449-453. (Pubitemid 23030937)
11. Connor J. D., (1975) Electrophysiology of the nigro-caudate dopamine pathway. Pharmacol. Ther. B. 1, 357-370.
12. Cragg S. J., and, Rice M. E., (2004) DAncing past the DAT at a DA synapse. Trends Neurosci. 27, 270-277. (Pubitemid 38529955)
13. Curet O., De Montigny C., and, Blier P., (1992) Effect of desipramine and amphetamine on noradrenergic neurotransmission: electrophysiological studies in the rat brain. Eur. J. Pharmacol. 221, 59-70.
14. Dugast C., Suaudchagny M. F., and, Gonon F., (1994) Continuous in-vivo monitoring of evoked dopamine release in the rat nucleus-accumbens by amperometry. Neuroscience 62, 647-654. (Pubitemid 24325643)
15. Dugast C., Cespuglio R., and, Suaud-Chagny M. F., (2002) In vivo monitoring of evoked noradrenaline release in the rat anteroventral thalamic nucleus by continuous amperometry. J. Neurochem. 82, 529-537. (Pubitemid 34831492)
16. Fa M., Mereu G., Ghiglieri V., Meloni A., Salis P., and, Gessa G. L., (2003) Electrophysiological and pharmacological characteristics of nigral dopaminergic neurons in the conscious, head-restrained rat. Synapse 48, 1-9. (Pubitemid 36249885)
17. Foote S. L., Aston-Jones G., and, Bloom F. E., (1980) Impulse activity of locus coeruleus neurons in awake rats and monkeys is a function of sensory stimulation and arousal. Proc. Natl. Acad. Sci. USA 77, 3033-3037. (Pubitemid 10031725)
18. Forray M. I., and, Gysling K., (2004) Role of noradrenergic projections to the bed nucleus of the stria terminalis in the regulation of the hypothalamic-pituitary-adrenal axis. Brain Res. Rev. 47, 145-160. (Pubitemid 39574317)
19. Garguilo M. G., and, Michael A. C., (1996) Amperometric microsensors for monitoring choline in the extracellular fluid of brain. J. Neurosci. Methods 70, 73-82. (Pubitemid 26411440)
20. Garris P. A., and, Wightman R. M., (1994) In vivo voltammetric measurement of evoked extracellular dopamine in the rat basolateral amygdaloid nucleus. J. Physiol. 478 (Pt 2), 239-249. (Pubitemid 24232196)
21. Garris P. A., and, Wightman R. M., (1995a) Distinct pharmacological regulation of evoked dopamine efflux in the amygdala and striatum of the rat in-vivo. Synapse 20, 269-279.
22. Garris P. A., and, Wightman R. M., (1995b) Regional differences in dopamine release, uptake, and diffusion measured by fast-scan cyclic voltammetry, in Voltammetric Methods in Brain Systems (, Boulton A., Baker G., and, Adams R. N., eds), pp. 179-220. Humana, Totowa, NJ.
23. Grace A. A., and, Bunney B. S., (1983) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons-1. Identification and characterization. Neuroscience 10, 301-315. (Pubitemid 13019570)
24. Harley C. W., (2004) Norepinephrine and dopamine as learning signals. Neural. Plast. 11, 191-204. (Pubitemid 40123736)
25. Heien M. L. A. V., Phillips P. E. M., Stuber G. D., Seipel A. T., and, Wightman R. M., (2003) Overoxidation of carbon-fiber microelectrodes enhances dopamine adsorption and increases sensitivity. Analyst 128, 1413-1419. (Pubitemid 38082985)
26. Heien M. L. A. V., Johnson M. A., and, Wightman R. M., (2004) Resolving neurotransmitters detected by fast-scan cyclic voltammetry. Anal. Chem. 76, 5697-5704. (Pubitemid 39313316)
27. Hermans A., Keithley R. B., Kita J. M., Sombers L. A., and, Wightman R. M., (2008) Dopamine detection with fast-scan cyclic voltammetry used with analog background subtraction. Anal. Chem. 80, 4040-4048. (Pubitemid 351812754)
28. Keithley R. B., Heien M. L., and, Wightman R. M., (2009) Multivariate concentration determination using principal component regression with residual analysis. Trac-Trends Anal. Chem. 28, 1127-1136.
29. Kilts C. D., and, Anderson C. M., (1986) The simultaneous quantification of dopamine, norepinephrine and epinephrine in micropunched rat brain nuclei by on-line trace enrichment HPLC with electrochemical detection: Distribution of catecholamines in the limbic system. Neurochem. Int. 9, 437-445. (Pubitemid 16018406)
30. Kita J. M., Parker L. E., Phillips P. E., Garris P. A., and, Wightman R. M., (2007) Paradoxical modulation of short-term facilitation of dopamine release by dopamine autoreceptors. J. Neurochem. 102, 1115-1124. (Pubitemid 47174232)
31. Kizer J. S., Kopin I. J., and, Zivin J. A., (1975) Proceedings: estimates of catecholamine turnover rates in individual hypothalamic nuclei of the rat by use of alpha-methyl-para-tyrosine. Br. J. Pharmacol. 54, 243P.
32. Kuczenski R., Melega W. P., Cho A. K., and, Segal D. S., (1997) Extracellular dopamine and amphetamine after systemic amphetamine administration: comparison to the behavioral response. J. Pharmacol. Exp. Ther. 282, 591-596. (Pubitemid 27340156)
33. L'Heureux R., Dennis T., Curet O., and, Scatton B., (1986) Measurement of endogenous noradrenaline release in the rat cerebral cortex in vivo by transcortical dialysis: effects of drugs affecting noradrenergic transmission. J. Neurochem. 46, 1794-1801. (Pubitemid 16095486)
34. Lu Y., Peters J. L., and, Michael A. C., (1998) Direct comparison of the response of voltammetry and microdialysis to electrically evoked release of striatal dopamine. J. Neurochem. 70, 584-593. (Pubitemid 28079347)
35. McMillen B. A., German D. C., and, Shore P. A., (1980) Functional and pharmacological significance of brain dopamine and norepinephrine storage pools. Biochem. Pharmacol. 29, 3045-3050. (Pubitemid 10029604)
36. Michael D. J., Joseph J. D., Kilpatrick M. R., Travis E. R., and, Wightman R. M., (1999) Improving data acquisition for fast scan cyclic voltammetry. Anal. Chem. 71, 3941-3947.
37. Millar J., Stamford J. A., Kruk Z. L., and, Wightman R. M., (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, 341-348. (Pubitemid 15108982)
38. Mitchell K., and, Adams R. N., (1993) Comparison of the effects of voltage-sensitive calcium-channel antagonism on the electrically stimulated release of dopamine and norepinephrine invivo. Brain Res. 604, 349-353. (Pubitemid 23080136)
39. Mitchell K., Oke A. F., and, Adams R. N., (1994) In-vivo dynamics of norepinephrine release reuptake in multiple terminal field regions of rat-brain. J. Neurochem. 63, 917-926. (Pubitemid 24266604)
40. Miyahara S., and, Oomura Y., (1982) Inhibitory-action of the ventral noradrenergic bundle on the lateral hypothalamic neurons through alpha-noradrenergic mechanisms in the rat. Brain Res. 234, 459-463. (Pubitemid 12175913)
41. Moore R. Y., and, Bloom F. E., (1978) Central catecholamine neuron systems: anatomy and physiology of the dopamine systems. Annu. Rev. Neurosci. 1, 129-169.
42. Nakamura S., Tepper J. M., Young S. J., and, Groves P. M., (1982) Changes in noradrenergic terminal excitability induced by amphetamine and their relation to impulse traffic. Neuroscience 7, 2217-2224. (Pubitemid 12034585)
43. Okada M., Mine K., and, Fujiwara M., (1990) Differential calcium dependence between the release of endogenous dopamine and noradrenaline from rat brain synaptosomes. J. Neurochem. 54, 1947-1952.
44. Onaka T., and, Yagi K., (1998) Role of noradrenergic projections to the bed nucleus of the stria terminalis in neuroendocrine and behavioral responses to fear-related stimuli in rats. Brain Res. 788, 287-293. (Pubitemid 28202172)
45. Owesson-White C. A., Cheer J. F., Beyene M., Carelli R. M., and, Wightman R. M., (2008) Dynamic changes in accumbens dopamine correlate with learning during intracranial self-stimulation. Proc. Natl. Acad. Sci. USA 105, 11957-11962.
46. Parikh V., Pomerleau F., Huettl P., Gerhardt G. A., Sarter M., and, Bruno J. P., (2004) Rapid assessment of in vivo cholinergic transmission by amperometric detection of changes in extracellular choline levels. Eur. J. Neurosci. 20, 1545-1554. (Pubitemid 39274038)
47. Park J., Galligan J. J., Fink G. D., and, Swain G. M., (2006) In vitro continuous amperometry with a diamond microelectrode coupled with video microscopy for simultaneously monitoring endogenous norepinephrine and its effect on the contractile response of a rat mesenteric artery. Anal. Chem. 78, 6756-6764. (Pubitemid 44522525)
48. Park J., Kile B. M., and, Wightman R. M., (2009) In vivo voltammetric monitoring of norepinephrine release in the rat ventral bed nucleus of the stria terminalis and anteroventral thalamic nucleus. Eur. J. Neuro. 30, 2121-2133.
49. Park J., Aragona B. J., Kile B. M., Carelli R. M., and, Wightman R. M., (2010) In vivo voltammetric monitoring of catecholamine release in subterritories of the nucleus accumbens shell. Neuroscience 169, 132-142.
50. Paxinos G., (1995) The Rat Nervous System. Academic Press, San Diego.
51. Paxinos G., and, Watson C., (2007) The Rat Brain in Stereotaxic Coordinates. Academic Press/Elsevier, Amsterdam; Boston.
52. Phelix C. F., Liposits Z., and, Paull W. K., (1992) Monoamine innervation of bed nucleus of stria terminalis: an electron microscopic investigation. Brain Res. Bull. 28, 949-965.
53. Phillips P. E. M., and, Wightman R. M., (2003) Critical guidelines for validation of the selectivity of in-vivo chemical microsensors. Trac-Trends Anal. Chem. 22, 509-514. (Pubitemid 37088219)
54. Raiteri M., Levi G., and, Federico R., (1974) d-amphetamine and the release of 3H-norepinephrine from synaptosomes. Eur. J. Pharmacol., 28, 237-240.
55. Ramsson E. S., Covey D. P., Daberkow D. P., Litherland M. T., Juliano S. A., and, Garris P. A., (2011) Amphetamine augments action potential-dependent dopaminergic signaling in the striatum in vivo. J. Neurochem. 117, 937-948.
56. Ranck J. B., (1975) Which elements are excited in electrical-stimulation of mammalian central nervous-system-review. Brain Res. 98, 417-440.
57. Robinson D. L., Hermans A., Seipel A. T., and, Wightman R. M., (2008) Monitoring rapid chemical communication in the brain. Chem. Rev. 108, 2554-2584.
58. Rothman R. B., and, Baumann M. H., (2003) Monoamine transporters and psychostimulant drugs. Eur. J. Pharmacol. 479, 23-40. (Pubitemid 37377873)
59. Ryan L. J., Tepper J. M., Young S. J., and, Groves P. M., (1985) Amphetamine's effects on terminal excitability of noradrenergic locus coeruleus neurons are impulse-dependent at low but not high doses. Brain Res. 341, 155-163. (Pubitemid 15246333)
60. Sanghera M. K., German D. C., Kiser R. S., and, Shore P. A., (1979) Differences in norepinephrine and dopamine neurotransmitter storage systems. Brain Res. Bull. 4, 217-221. (Pubitemid 9215987)
61. Saphier D., (1993) Electrophysiology and neuropharmacology of noradrenergic projections to rat PVN magnocellular neurons. Am. J. Physiol. 264, R891-R902. (Pubitemid 23152570)
62. Shi W. X., Pun C. L., Zhang X. X., Jones M. D., and, Bunney B. S., (2000) Dual effects of D-amphetamine on dopamine neurons mediated by dopamine and nondopamine receptors. J. Neurosci. 20, 3504-3511. (Pubitemid 30263765)
63. Shi W. X., Zhang X. Y., Pun C. L., and, Bunney B. S., (2007) Clozapine blocks D-amphetamine-induced excitation of dopamine neurons in the ventral tegmental area. Neuropsychopharmacology 32, 1922-1928. (Pubitemid 47258526)
64. Shimizu N., Duan S. M., Hori T., and, Oomura Y., (1990) Glutamate modulates dopamine release in the striatum as measured by brain microdialysis. Brain Res. Bull. 25, 99-102. (Pubitemid 20246620)
65. Stamford J. A., and, Justice J. B., Jr, (1996) Probing brain chemistry. Anal. Chem. 68, 359A-363A.
66. Sulzer D., Sonders M. S., Poulsen N. W., and, Galli A., (2005) Mechanisms of neurotransmitter release by amphetamines: a review. Prog. Neurobiol. 75, 406-433. (Pubitemid 40834286)
67. Takmakov P., Zachek M. K., Keithley R. B., Bucher E. S., McCarty G. S., and, Wightman R. M., (2010) Characterization of local pH changes in brain using fast-scan cyclic voltammetry with carbon microelectrodes. Anal. Chem. 82, 9892-9900.
68. Takmakov P., McKinney C. J., Carelli R. M., and, Wightman R. M., (2011) Instrumentation for fast-scan cyclic voltammetry combined with electrophysiology for behavioral experiments in freely moving animals. Rev. Sci. Instrum. 82, 074302.
69. Ungerstedt U., (1971) Stereotaxic mapping of monoamine pathways in rat brain. Acta Physiol. Scand. Suppl. 367, 1-48.
70. Venton B. J., and, Wightman R. M., (2007) Pharmacologically induced, subsecond dopamine transients in the caudate-putamen of the anesthetized rat. Synapse 61, 37-39. (Pubitemid 44924657)
71. Weinshenker D., and, Schroeder J. P., (2007) There and back again: a tale of norepinephrine and drug addiction. Neuropsychopharmacology 32, 1433-1451. (Pubitemid 46920149)
72. Widerlov E., and, Lewander T., (1978) Inhibition of the in vivo biosynthesis and changes of catecholamine levels in rat brain after alpha-methyl-p-tyrosine; time- and dose-response relationships. Naunyn Schmiedebergs Arch. Pharmacol. 304, 111-123. (Pubitemid 9013999)
73. Wiedemann D. J., Kawagoe K. T., Kennedy R. T., Ciolkowski E. L., and, Wightman R. M., (1991) Strategies for low detection limit measurements with cyclic voltammetry. Anal. Chem. 63, 2965-2970.
74. Wightman R. M., Amatore C., Engstrom R. C., Hale P. D., Kristensen E. W., Kuhr W. G., and, May L. J., (1988) Real-time characterization of dopamine overflow and uptake in the rat striatum. Neuroscience 25, 513-523.
75. Zachek M. K., Takmakov P., Moody B., Wightman R. M., and, McCarty G. S., (2009) Simultaneous decoupled detection of dopamine and oxygen using pyrolyzed carbon microarrays and fast-scan cyclic voltammetry. Anal. Chem. 81, 6258-6265.
76. Zachek M. K., Takmakov P., Park J., Wightman R. M., and, McCarty G. S., (2010) Simultaneous monitoring of dopamine concentration at spatially different brain locations in vivo. Biosens. Bioelectron. 25, 1179-1185.