Monitoring serotonin signaling on a subsecond time scale

Frontiers in Integrative Neuroscience

Volumn , Issue MAY, 2013, Pages

  Dankoski, Elyse C ^a   Mark Wightman, R ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

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

Author keywords

5 HT; Carbon fiber microelectrode; Cyclic voltammetry; Selective serotonin reuptake inhibitor; Serotonin autoreceptor; Serotonin transporter

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING); FLUOXETINE; PAROXETINE; SEROTONIN; SEROTONIN 1A RECEPTOR; SEROTONIN 1B RECEPTOR; SEROTONIN 1D RECEPTOR; SEROTONIN TRANSPORTER; SEROTONIN UPTAKE INHIBITOR; VESICULAR MONOAMINE TRANSPORTER 2;

BRAIN SLICE; CYCLIC POTENTIOMETRY; DEPRESSION; DORSAL RAPHE NUCLEUS; ELECTROCHEMICAL ANALYSIS; ELECTROSTIMULATION; FAST SCAN CYCLIC VOLTAMMETRY; HUMAN; LATERAL GENICULATE BODY; LONG TERM EXPOSURE; MEDIAL FOREBRAIN BUNDLE; NEUROLOGIC DISEASE; NEUROMODULATION; NONHUMAN; REVIEW; SEROTONIN BRAIN LEVEL; SEROTONIN RELEASE; SEROTONIN UPTAKE; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; SEROTONINERGIC TRANSMISSION; SUPRACHIASMATIC NUCLEUS;

EID: 84877999524     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2013.00044     Document Type: Review

References (104)

1. Adell, A., Celada, P., and Artigas, F. (2001). The role of 5-HT1B receptors in the regulation of serotonin cell firing and release in the rat brain. J Neurochem 79, 172-182.
2. Aghajanian, G.K., Sprouse, J.S., Sheldon, P., and Rasmussen, K. (1990). Electrophysiology of the central serotonin system: receptor subtypes and transducer mechanisms. Ann N Y Acad Sci 600, 93-103; discussion 103.
3. Aghajanian, G.K., Wang, R.Y., and Baraban, J. (1978). Serotonergic and non-serotonergic neurons of the dorsal raphe: reciprocal changes in firing induced by peripheral nerve stimulation. Brain Res 153, 169-175.
4. Anden, N.E., Fuxe, K., and Ungerstedt, U. (1967). Monoamine pathways to the cerebellum and cerebral cortex. Experientia 23, 838-839.
5. Artigas, F., Perez, V., and Alvarez, E. (1994). Pindolol induces a rapid improvement of depressed patients treated with serotonin reuptake inhibitors. Arch Gen Psychiatry 51, 248-251.
6. Barnes, N.M., and Sharp, T. (1999). A review of central 5-HT receptors and their function. Neuropharmacology 38, 1083-1152.
7. Bel, N., and Artigas, F. (1992). Fluvoxamine preferentially increases extracellular 5-hydroxytryptamine in the raphe nuclei: an in vivo microdialysis study. Eur J Pharmacol 229, 101-103.
8. Bennett, J.P., Jr., Logan, W.J., and Snyder, S.H. (1973). Amino acids as central nervous transmitters: the influence of ions, amino acid analogues, and ontogeny on transport systems for L-glutamic and L-aspartic acids and glycine into central nervous synaptosomes of the rat. J Neurochem 21, 1533-1550.
9. Blakely, R.D., Berson, H.E., Fremeau, R.T., Jr., Caron, M.G., Peek, M.M., Prince, H.K., and Bradley, C.C. (1991). Cloning and expression of a functional serotonin transporter from rat brain. Nature 354, 66-70.
10. Blier, P., De Montigny, C., and Chaput, Y. (1987). Modifications of the serotonin system by antidepressant treatments: implications for the therapeutic response in major depression. J Clin Psychopharmacol 7, 24S-35S.
11. Blier, P., De Montigny, C., and Chaput, Y. (1988). Electrophysiological assessment of the effects of antidepressant treatments on the efficacy of 5-HT neurotransmission. Clin Neuropharmacol 11 Suppl 2, S1-10.
12. Blier, P., De Montigny, C., and Chaput, Y. (1990). A role for the serotonin system in the mechanism of action of antidepressant treatments: preclinical evidence. J Clin Psychiatry 51 Suppl, 14-20; discussion 21.
13. Boess, F.G., and Martin, I.L. (1994). Molecular biology of 5-HT receptors. Neuropharmacology 33, 275-317.
14. Bortolozzi, A., Castane, A., Semakova, J., Santana, N., Alvarado, G., Cortes, R., Ferres-Coy, A., Fernandez, G., Carmona, M.C., Toth, M., Perales, J.C., Montefeltro, A., and Artigas, F. (2011). Selective siRNA-mediated suppression of 5-HT(1A) autoreceptors evokes strong anti-depressant-like effects. Mol Psychiatry.
15. Borue, X., Condron, B., and Venton, B.J. (2010). Both synthesis and reuptake are critical for replenishing the releasable serotonin pool in Drosophila. J Neurochem 113, 188-199.
16. Borue, X., Cooper, S., Hirsh, J., Condron, B., and Venton, B.J. (2009). Quantitative evaluation of serotonin release and clearance in Drosophila. J Neurosci Methods 179, 300-308.
17. Bosker, F.J., Cremers, T.I., Jongsma, M.E., Westerink, B.H., Wikstrom, H.V., and Den Boer, J.A. (2001). Acute and chronic effects of citalopram on postsynaptic 5-hydroxytryptamine(1A) receptor-mediated feedback: a microdialysis study in the amygdala. J Neurochem 76, 1645-1653.
18. Bosker, F.J., Klompmakers, A.A., and Westenberg, H.G. (1995a). Effects of single and repeated oral administration of fluvoxamine on extracellular serotonin in the median raphe nucleus and dorsal hippocampus of the rat. Neuropharmacology 34, 501-508.
19. Bosker, F.J., Van Esseveldt, K.E., Klompmakers, A.A., and Westenberg, H.G. (1995b). Chronic treatment with fluvoxamine by osmotic minipumps fails to induce persistent functional changes in central 5-HT1A and 5-HT1B receptors, as measured by in vivo microdialysis in dorsal hippocampus of conscious rats. Psychopharmacology (Berl) 117, 358-363.
20. Brazell, M.P., Kasser, R.J., Renner, K.J., Feng, J., Moghaddam, B., and Adams, R.N. (1987). Electrocoating carbon fiber microelectrodes with Nafion improves selectivity for electroactive neurotransmitters. J Neurosci Methods 22, 167-172.
21. Bunin, M.A., Prioleau, C., Mailman, R.B., and Wightman, R.M. (1998). Release and uptake rates of 5-hydroxytryptamine in the dorsal raphe and substantia nigra reticulata of the rat brain. J Neurochem 70, 1077-1087.
22. Bunin, M.A., and Wightman, R.M. (1998). Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission. J Neurosci 18, 4854-4860.
23. Casanovas, J.M., Lesourd, M., and Artigas, F. (1997). The effect of the selective 5-HT1A agonists alnespirone (S-20499) and 8-OH-DPAT on extracellular 5-hydroxytryptamine in different regions of rat brain. Br J Pharmacol 122, 733-741.
24. Cases, O., Lebrand, C., Giros, B., Vitalis, T., De Maeyer, E., Caron, M.G., Price, D.J., Gaspar, P., and Seif, I. (1998). Plasma membrane transporters of serotonin, dopamine, and norepinephrine mediate serotonin accumulation in atypical locations in the developing brain of monoamine oxidase A knock-outs. J Neurosci 18, 6914-6927.
25. Cases, O., Seif, I., Grimsby, J., Gaspar, P., Chen, K., Pournin, S., Muller, U., Aguet, M., Babinet, C., Shih, J.C., and et al. (1995). Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268, 1763-1766.
26. Chaput, Y., De Montigny, C., and Blier, P. (1986). Effects of a selective 5-HT reuptake blocker, citalopram, on the sensitivity of 5-HT autoreceptors: electrophysiological studies in the rat brain. Naunyn Schmiedebergs Arch Pharmacol 333, 342-348.
27. Chazal, G., and Ralston, H.J., 3rd (1987). Serotonin-containing structures in the nucleus raphe dorsalis of the cat: an ultrastructural analysis of dendrites, presynaptic dendrites, and axon terminals. J Comp Neurol 259, 317-329.
28. Clarke, W.P., Yocca, F.D., and Maayani, S. (1996). Lack of 5-hydroxytryptamine1A-mediated inhibition of adenylyl cyclase in dorsal raphe of male and female rats. J Pharmacol Exp Ther 277, 1259-1266.
29. Cragg, S.J., Hawkey, C.R., and Greenfield, S.A. (1997). Comparison of serotonin and dopamine release in substantia nigra and ventral tegmental area: region and species differences. J Neurochem 69, 2378-2386.
30. Cremers, T.I., Spoelstra, E.N., De Boer, P., Bosker, F.J., Mork, A., Den Boer, J.A., Westerink, B.H., and Wikstrom, H.V. (2000). Desensitisation of 5-HT autoreceptors upon pharmacokinetically monitored chronic treatment with citalopram. Eur J Pharmacol 397, 351-357
31. Davidson, C., and Stamford, J.A. (1995a). The effect of paroxetine on 5-HT efflux in the rat dorsal raphe nucleus is potentiated by both 5-HT1A and 5-HT1B/D receptor antagonists. Neurosci Lett 188, 41-44.
32. Davidson, C., and Stamford, J.A. (1995b). Evidence that 5-hydroxytryptamine release in rat dorsal raphe nucleus is controlled by 5-HT1A, 5-HT1B and 5-HT1D autoreceptors. Br J Pharmacol 114, 1107-1109.
33. Davidson, C., and Stamford, J.A. (1996). Serotonin efflux in the rat ventral lateral geniculate nucleus assessed by fast cyclic voltammetry is modulated by 5-HT1B and 5-HT1D autoreceptors. Neuropharmacology 35, 1627-1634.
34. Davidson, C., and Stamford, J.A. (1997). Synergism of 5-HT 1B/D antagonists with paroxetine on serotonin efflux in rat ventral lateral geniculate nucleus slices. Brain Res Bull 43, 405-409.
35. Davidson, C., and Stamford, J.A. (1998). Contrasting effects of chronic paroxetine on 5-HT1A control of dorsal raphe cell firing and 5-HT release. Neuroreport 9, 2535-2538.
36. Davidson, C., and Stamford, J.A. (2000). Effect of chronic paroxetine treatment on 5-HT1B and 5-HT1D autoreceptors in rat dorsal raphe nucleus. Neurochem Int 36, 91-96.
37. Daws, L.C. (2009). Unfaithful neurotransmitter transporters: focus on serotonin uptake and implications for antidepressant efficacy. Pharmacol Ther 121, 89-99.
38. Day, H.E., Greenwood, B.N., Hammack, S.E., Watkins, L.R., Fleshner, M., Maier, S.F., and Campeau, S. (2004). Differential expression of 5HT-1A, alpha 1b adrenergic, CRF-R1, and CRF-R2 receptor mRNA in serotonergic, gamma-aminobutyric acidergic, and catecholaminergic cells of the rat dorsal raphe nucleus. J Comp Neurol 474, 364-378.
39. Descarries, L., Audet, M.A., Doucet, G., Garcia, S., Oleskevich, S., Seguela, P., Soghomonian, J.J., and Watkins, K.C. (1990). Morphology of central serotonin neurons. Brief review of quantified aspects of their distribution and ultrastructural relationships. Ann N Y Acad Sci 600, 81-92.
40. Dong, S., Allen, J.A., Farrell, M., and Roth, B.L. (2010). A chemical-genetic approach for precise spatio-temporal control of cellular signaling. Mol Biosyst 6, 1376-1380.
41. Evrard, A., Malagie, I., Laporte, A.M., Boni, C., Hanoun, N., Trillat, A.C., Seif, I., De Maeyer, E., Gardier, A., Hamon, M., and Adrien, J. (2002). Altered regulation of the 5-HT system in the brain of MAO-A knock-out mice. Eur J Neurosci 15, 841-851.
42. Fuxe, K. (1965). Evidence for the Existence of Monoamine Neurons in the Central Nervous System. Iv. Distribution of Monoamine Nerve Terminals in the Central Nervous System. Acta Physiol Scand Suppl, SUPPL 247:237+.
43. Fuxe, K., Dahlstrom, A.B., Jonsson, G., Marcellino, D., Guescini, M., Dam, M., Manger, P., and Agnati, L. (2010). The discovery of central monoamine neurons gave volume transmission to the wired brain. Prog Neurobiol 90, 82-100.
44. Gartside, S.E., Umbers, V., Hajos, M., and Sharp, T. (1995). Interaction between a selective 5-HT1A receptor antagonist and an SSRI in vivo: effects on 5-HT cell firing and extracellular 5-HT. Br J Pharmacol 115, 1064-1070.
45. Hagan, C.E., Schenk, J.O., and Neumaier, J.F. (2011). The contribution of low-affinity transport mechanisms to serotonin clearance in synaptosomes. Synapse 65, 1015-1023.
46. Hajos, M., Gartside, S.E., Villa, A.E., and Sharp, T. (1995). Evidence for a repetitive (burst) firing pattern in a sub-population of 5-hydroxytryptamine neurons in the dorsal and median raphe nuclei of the rat. Neuroscience 69, 189-197.
47. Hashemi, P., Dankoski, E.C., Lama, R., Wood, K.M., Takmakov, P., and Wightman, R.M. (2012). Brain dopamine and serotonin differ in regulation and its consequences. Proc Natl Acad Sci U S A 109, 11510-11515.
48. Hashemi, P., Dankoski, E.C., Petrovic, J., Keithley, R.B., and Wightman, R.M. (2009). Voltammetric detection of 5-hydroxytryptamine release in the rat brain. Anal Chem 81, 9462-9471.
49. Hashemi, P., Dankoski, E.C., Wood, K.M., Ambrose, R.E., and Wightman, R.M. (2011). In vivo electrochemical evidence for simultaneous 5-HT and histamine release in the rat substantia nigra pars reticulata following medial forebrain bundle stimulation. J Neurochem 118, 749-759.
50. Herr, N.R., and Wightman, R.M. (2013). Improved techniques for examining rapid dopamine signaling with iontophoresis. Front Biosci (Elite Ed) 5, 249-257.
51. Hjorth, S. (1993). Serotonin 5-HT1A autoreceptor blockade potentiates the ability of the 5-HT reuptake inhibitor citalopram to increase nerve terminal output of 5-HT in vivo: a microdialysis study. J Neurochem 60, 776-779.
52. Hjorth, S., and Sharp, T. (1991). Effect of the 5-HT1A receptor agonist 8-OH-DPAT on the release of 5-HT in dorsal and median raphe-innervated rat brain regions as measured by in vivo microdialysis. Life Sci 48, 1779-1786.
53. Hopwood, S.E., and Stamford, J.A. (2001). Multiple 5-HT(1) autoreceptor subtypes govern serotonin release in dorsal and median raphe nuclei. Neuropharmacology 40, 508-519.
54. Invernizzi, R., Belli, S., and Samanin, R. (1992). Citalopram's ability to increase the extracellular concentrations of serotonin in the dorsal raphe prevents the drug's effect in the frontal cortex. Brain Res 584, 322-324.
55. Invernizzi, R., Bramante, M., and Samanin, R. (1995). Extracellular concentrations of serotonin in the dorsal hippocampus after acute and chronic treatment with citalopram. Brain Res 696, 62-66.
56. Iravani, M.M., and Kruk, Z.L. (1997). Real-time measurement of stimulated 5-hydroxytryptamine release in rat substantia nigra pars reticulata brain slices. Synapse 25, 93-102.
57. Iravani, M.M., Muscat, R., and Kruk, Z.L. (1999). MK-801 interaction with the 5-HT transporter: a real-time study in brain slices using fast cyclic voltammetry. Synapse 32, 212-224.
58. Iversen, L.L. (1974). Uptake mechanisms for neurotransmitter amines. Biochem Pharmacol 23, 1927-1935.
59. Jackson, B.P., Dietz, S.M., and Wightman, R.M. (1995). Fast-scan cyclic voltammetry of 5-hydroxytryptamine. Anal Chem 67, 1115-1120.
60. Jennings, K.A., Lesch, K.P., Sharp, T., and Cragg, S.J. (2010). Non-linear relationship between 5-HT transporter gene expression and frequency sensitivity of 5-HT signals. J Neurochem 115, 965-973.
61. John, C.E., Budygin, E.A., Mateo, Y., and Jones, S.R. (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, 267-282.
62. Judge, S.J., and Gartside, S.E. (2006). Firing of 5-HT neurones in the dorsal and median raphe nucleus in vitro shows differential alpha1-adrenoceptor and 5-HT1A receptor modulation. Neurochem Int 48, 100-107.
63. Kia, H.K., Brisorgueil, M.J., Hamon, M., Calas, A., and Verge, D. (1996). Ultrastructural localization of 5-hydroxytryptamine1A receptors in the rat brain. J Neurosci Res 46, 697-708.
64. Kovacevic, T., Skelin, I., and Diksic, M. (2010). Chronic fluoxetine treatment has a larger effect on the density of a serotonin transporter in the Flinders Sensitive Line (FSL) rat model of depression than in normal rats. Synapse 64, 231-240.
65. Kovachich, G.B., Aronson, C.E., Brunswick, D.J., and Frazer, A. (1988). Quantitative autoradiography of serotonin uptake sites in rat brain using [3H]cyanoimipramine. Brain Res 454, 78-88.
66. Kreiss, D.S., and Lucki, I. (1994). Differential regulation of serotonin (5-HT) release in the striatum and hippocampus by 5-HT1A autoreceptors of the dorsal and median raphe nuclei. J Pharmacol Exp Ther 269, 1268-1279.
67. Kreiss, D.S., and Lucki, I. (1997). Chronic administration of the 5-HT1A receptor agonist 8-OH-DPAT differentially desensitizes 5-HT1A autoreceptors of the dorsal and median raphe nuclei. Synapse 25, 107-116.
68. Lama, R.D., Charlson, K., Anantharam, A., and Hashemi, P. (2012). Ultrafast detection and quantification of brain signaling molecules with carbon fiber microelectrodes. Anal Chem 84, 8096-8101.
69. Limberger, N., Trout, S.J., Kruk, Z.L., and 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, 623-629.
70. Merrill, E.G., Wall, P.D., and Yaksh, T.L. (1978). Properties of two unmyelinated fibre tracts of the central nervous system: lateral Lissauer tract, and parallel fibres of the cerebellum. J Physiol 284, 127-145.
71. 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.
72. Moret, C., and Briley, M. (1996). Effects of acute and repeated administration of citalopram on extracellular levels of serotonin in rat brain. Eur J Pharmacol 295, 189-197.
73. Moret, C., and Briley, M. (1997). 5-HT autoreceptors in the regulation of 5-HT release from guinea pig raphe nucleus and hypothalamus. Neuropharmacology 36, 1713-1723.
74. Moukhles, H., Bosler, O., Bolam, J.P., Vallee, A., Umbriaco, D., Geffard, M., and Doucet, G. (1997). Quantitative and morphometric data indicate precise cellular interactions between serotonin terminals and postsynaptic targets in rat substantia nigra. Neuroscience 76, 1159-1171.
75. O'connor, J.J., and Kruk, Z.L. (1991a). Fast cyclic voltammetry can be used to measure stimulated endogenous 5-hydroxytryptamine release in untreated rat brain slices. J Neurosci Methods 38, 25-33.
76. O'connor, J.J., and Kruk, Z.L. (1991b). Frequency dependence of 5-HT autoreceptor function in rat dorsal raphe and suprachiasmatic nuclei studied using fast cyclic voltammetry. Brain Res 568, 123-130.
77. O'connor, J.J., and Kruk, Z.L. (1992). Pharmacological characteristics of 5-hydroxytryptamine autoreceptors in rat brain slices incorporating the dorsal raphe or the suprachiasmatic nucleus. Br J Pharmacol 106, 524-532.
78. O'connor, J.J., and Kruk, Z.L. (1994). Effects of 21 days treatment with fluoxetine on stimulated endogenous 5-hydroxytryptamine overflow in the rat dorsal raphe and suprachiasmatic nucleus studied using fast cyclic voltammetry in vitro. Brain Res 640, 328-335.
79. Oh, E., Maejima, T., Liu, C., Deneris, E., and Herlitze, S. (2010). Substitution of 5-HT1A receptor signaling by a light-activated G protein-coupled receptor. J Biol Chem 285, 30825-30836.
80. Ohno, Y. (2010). New insight into the therapeutic role of 5-HT1A receptors in central nervous system disorders. Cent Nerv Syst Agents Med Chem 10, 148-157.
81. Owesson, C.A., Hopwood, S.E., Callado, L.F., Seif, I., Mclaughlin, D.P., and Stamford, J.A. (2002). Altered presynaptic function in monoaminergic neurons of monoamine oxidase-A knockout mice. Eur J Neurosci 15, 1516-1522.
82. Pazos, A., and Palacios, J.M. (1985). Quantitative autoradiographic mapping of serotonin receptors in the rat brain. I. Serotonin-1 receptors. Brain Res 346, 205-230.
83. Phillips, P.E., Hancock, P.J., and Stamford, J.A. (2002). Time window of autoreceptor-mediated inhibition of limbic and striatal dopamine release. Synapse 44, 15-22.
84. Pineyro, G., Castanon, N., Hen, R., and Blier, P. (1995). Regulation of [3H]5-HT release in raphe, frontal cortex and hippocampus of 5-HT1B knock-out mice. Neuroreport 7, 353-861
85. Roberts, C., and Price, G.W. (2001). Interaction of serotonin autoreceptor antagonists in the rat dorsal raphe nucleus: an in vitro fast cyclic voltammetry study. Neurosci Lett 300, 45-48.
86. Rossi, D.V., Burke, T.F., Mccasland, M., and Hensler, J.G. (2008). Serotonin-1A receptor function in the dorsal raphe nucleus following chronic administration of the selective serotonin reuptake inhibitor sertraline. J Neurochem 105, 1091-1099.
87. Sari, Y. (2004). Serotonin1B receptors: from protein to physiological function and behavior. Neurosci Biobehav Rev 28, 565-582.
88. Schoups, A., Dillen, L., Claeys, M., Duchateau, A., Verbeuren, T.J., and De Potter, W.P. (1986). Characterization of serotonin receptors and lack of effect of antidepressant therapy on monoamine functions in various regions of the rabbit brain. Eur J Pharmacol 126, 259-271.
89. Schultz, K.N., and Kennedy, R.T. (2008). Time-resolved microdialysis for in vivo neurochemical measurements and other applications. Annu Rev Anal Chem (Palo Alto Calif) 1, 627-661.
90. Sprouse, J.S., and Aghajanian, G.K. (1987). Electrophysiological responses of serotoninergic dorsal raphe neurons to 5-HT1A and 5-HT1B agonists. Synapse 1, 3-9.
91. Stamford, J.A. (1985). In vivo voltammetry: promise and perspective. Brain Res 357, 119-135.
92. Stamford, J.A., Davidson, C., Mclaughlin, D.P., and Hopwood, S.E. (2000). Control of dorsal raphe 5-HT function by multiple 5-HT(1) autoreceptors: parallel purposes or pointless plurality? Trends Neurosci 23, 459-465.
93. Stamford, J.A., Kruk, Z.L., and Millar, J. (1990). Striatal dopamine terminals release serotonin after 5-HTP pretreatment: in vivo voltammetric data. Brain Res 515, 173-180.
94. Stamford, J.A., Kruk, Z.L., Millar, J., and Wightman, R.M. (1984). Striatal dopamine uptake in the rat: in vivo analysis by fast cyclic voltammetry. Neurosci Lett 51, 133-138.
95. 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.
96. Thienprasert, A., and Singer, E.A. (1993). Electrically induced release of endogenous noradrenaline and dopamine from brain slices: pseudo-one-pulse stimulation utilized to study presynaptic autoinhibition. Naunyn Schmiedebergs Arch Pharmacol 348, 119-126.
97. Threlfell, S., Greenfield, S.A., and Cragg, S.J. (2010). 5-HT(1B) receptor regulation of serotonin (5-HT) release by endogenous 5-HT in the substantia nigra. Neuroscience 165, 212-220.
98. Van Der Kooy, D., and Hattori, T. (1980). Dorsal raphe cells with collateral projections to the caudate-putamen and substantia nigra: a fluorescent retrograde double labeling study in the rat. Brain Res 186, 1-7.
99. Vandermaelen, C.P., and Aghajanian, G.K. (1983). Electrophysiological and pharmacological characterization of serotonergic dorsal raphe neurons recorded extracellularly and intracellularly in rat brain slices. Brain Res 289, 109-119.
100. Verge, D., Daval, G., Marcinkiewicz, M., Patey, A., El Mestikawy, S., Gozlan, H., and Hamon, M. (1986). Quantitative autoradiography of multiple 5-HT1 receptor subtypes in the brain of control or 5,7-dihydroxytryptamine-treated rats. J Neurosci 6, 3474-3482.
101. Verge, D., Daval, G., Patey, A., Gozlan, H., El Mestikawy, S., and Hamon, M. (1985). Presynaptic 5-HT autoreceptors on serotonergic cell bodies and/or dendrites but not terminals are of the 5-HT1A subtype. Eur J Pharmacol 113, 463-464.
102. 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.
103. Yocca, F.D., and Maayani, S. (1990). 5-HT receptors linked to adenylyl cyclase activity in mammalian brain. Ann N Y Acad Sci 600, 212-223.
104. Zhou, F.C., Tao-Cheng, J.H., Segu, L., Patel, T., and Wang, Y. (1998). Serotonin transporters are located on the axons beyond the synaptic junctions: anatomical and functional evidence. Brain Res 805, 241-254.