[en] A commonly held view is that dopamine exerts its effects via binding to D1- and D2-dopaminergic receptors. However, recent data have emerged supporting the existence of a direct interaction of dopamine with adrenergic but this interaction has been poorly investigated. In this study, the pharmacological basis of possible in vivo interactions between dopamine and alpha(2)-adrenergic receptors was investigated in zebra finches. A binding competition study showed that dopamine displaces the binding of the alpha(2)-adrenergic ligand, [(3)H]RX821002, in the brain. The affinity of dopamine for the adrenergic sites does not differ between the sexes and is 10- to 28-fold lower than that for norepinephrine. To assess the anatomical distribution of this interaction, binding competitions were performed on brain slices incubated in 5nM [(3)H]RX821002 in the absence of any competitor or in the presence of norepinephrine [0.1microM] or dopamine [1microM]. Both norepinephrine and dopamine displaced the binding of the radioligand though to a different extent in most of the regions studied (e.g., area X, the lateral part of the magnocellular nucleus of anterior nidopallium, HVC, arcopallium dorsale, ventral tegmental area and substantia grisea centralis) but not in the robust nucleus of the arcopallium. Together these data provide evidence for a direct interaction between dopamine and adrenergic receptors in songbird brains albeit with regional variation.
Disciplines :
Neurosciences & behavior
Author, co-author :
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Castelino, Christina B
Ball, Gregory F
Language :
English
Title :
Dopamine binds to alpha(2)-adrenergic receptors in the song control system of zebra finches (Taeniopygia guttata).
Aguayo L.G., and Grossie J. Dopamine inhibits a sustained calcium current through activation of alpha adrenergic receptors and a GTP-biding protein in adult rat sympathetic neurons. J. Pharm. Exp. Ther. 269 (1994) 503-508
Appeltants D., Absil P., Balthazart J., and Ball G.F. Identification of the origin of catecholaminergic inputs to HVc in canaries by retrograde tract tracing combined with tyrosine hydroxylase immunocytochemistry. J. Chem. Neuroanat. 18 (2000) 117-133
Appeltants D., Ball G.F., and Balthazart J. The distribution of tyrosine hydroxylase in the canary brain: demonstration of a specific and sexually dimorphic catecholaminergic innervation of the telencephalic song control nuclei. Cell Tissue Res. 304 (2001) 237-259
Appeltants D., Ball G.F., and Balthazart J. The origin of catecholaminergic inputs to the song control nucleus RA in canaries. Neuroreport 13 (2002) 649-653
Aston-Jones G., and Cohen J.D. An integrative theory of Locus coeruleus-Norepinephrine function: adaptative gain and optimal performance. Annu. Rev. Neurosci. 28 (2005) 403-450
Ball G.F. Neurochemical specializations associated with vocal learning and production in songbirds and budgerigars. Brain Behav. Evol. 44 (1994) 234-246
Ball G.F., and Balthazart J. The neuroendocrinology and neurochemistry of birdsong. In: Blaustein J.D. (Ed). Handbook of Neurochemistry and Molecular Biology-Behavioral Neurochemistry, Neuroendocrinology and Molecular Neurobiology. third ed. (2007), Plenum Press, New York 419-458
Ball G.F., Casto J.M., and Balthazart J. Autoradiographic localization of D1-like dopamine receptors in the forebrain of male and female Japanese quail and their relationship with immunoreactive tyrosine hydroxylase. J. Chem. Neuroanat. 9 (1995) 121-133
Ball G.F., Nock B., McEwen B.S., and Balthazart J. Distribution of alpha2-adrenergic receptors in the brain of the Japanese quail as determined by quantitative autoradiography: implications for the control of sexually dimorphic reproductive processes. Brain Res. 491 (1989) 68-79
Balthazart J., and Ball G.F. Effects of the noradrenergic neurotoxin DSP-4 on luteinizing hormone levels, catecholamine concentrations, alpha 2-adrenergic receptor binding, and aromatase activity in the brain of the Japanese quail. Brain Res. 492 (1989) 163-175
Barclay S.R., and Harding C.F. Androstenedione modulation of monoamine levels and turnover in hypothalamic and vocal control nuclei in the male zebra finch: steroid effects on brain monoamines. Brain Res. 459 (1988) 333-343
Barclay S.R., and Harding C.F. Differential modulation of monoamine levels and turnover rates by estrogen and/or androgen in hypothalamic and vocal control nuclei of male zebra finches. Brain Res. 523 (1990) 251-262
Barclay S.R., Harding C.F., and Waterman S.A. Correlations between catecholamine levels and sexual behavior in male zebra finches. Pharmacol. Biochem. Behav. 41 (1992) 195-201
Barclay S.R., Harding C.F., and Waterman S.A. Central DSP-4 treatment decreases norepinephrine levels and courtship behavior in male zebra finches. Pharmacol. Biochem. Behav. 53 (1996) 213-220
Berridge C.W., and Waterhouse B.D. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res. Brain Res. Rev. 42 (2003) 33-84
Bottjer S.W. The distribution of tyrosine hydroxylase immunoreactivity in the brains of male and female zebra finches. J. Neurobiol. 24 (1993) 51-69
Boyajian C.L., Loughlin S.E., and Leslie F.M. Anatomical evidence for alpha-2 adrenoceptor heterogeneity: differential autoradiographic distribution of [3H]Rauwolscine and [3H]idazoxan in rat brain. J. Pharmacol. Exp. Ther. 241 (1987) 1079-1091
Brainard M.S., and Doupe A.J. What songbirds teach us about learning. Nature 417 (2002) 351-358
Brenowitz E.A., and Beecher M.D. Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci. 28 (2005) 127-131
Brenowitz E.A., Margoliash D., and Nordeen K.W. An introduction to birdsong and the avian song system. J. Neurobiol. 33 (1997) 495-500
Bunemann M., Bucheler M.M., Philipp M., Lohse M.J., and Hein L. Activation and deactivation kinetics of alpha 2A- and alpha 2C-adrenergic receptor-activated G protein-activated inwardly rectifying K+ channel currents. J. Biol. Chem. 276 (2001) 47512-47517
Bylund D.B., Eikenberg D.C., Hieble J.P., Langer S.Z., Lefkowitz R.J., Minneman K.P., Molinoff P.B., Ruffolo R.R.J., and Trendelenburg U. IV. International union of pharmacology nomenclature of adrenoceptors. Pharmacol. Rev. 46 (1994) 121-136
Callier S., Snapyan M., Le Crom S., Prou D., Vincent J.-D., and Vernier P. Evolution of cell biology of dopamine receptors in vertebrates. Biol. Cell 95 (2003) 489-502
Carboni E., Tanda G.L., Frau R., and Di Chiara G. Blockade of the noradrenaline carrier increases extracellular dopamine concentrations in the prefrontal cortex: evidence that dopamine is taken up in vivo by noradrenergic terminals. J. Neurochem. 55 (1990) 1067-1070
Carboni E., Spielewoy C., Vacca C., Nosten-Bertrand M., Giros B., and Di Chiara G. Cocaine and amphetamine increase extracellular dopamine in the nucleus accumbens of mice lacking the dopamine transporter gene. J. Neurosci. 21 RC141 (2001) 1-4
Castelino C.B., and Ball G.F. A role for norepinephrine in the regulation of context-dependent ZENK expression in male zebra finches (Taeniopygia guttata). Eur. J. Neurosci. 21 (2005) 1962-1972
Castelino C.B., Diekamp B., and Ball G.F. Noradrenergic projections to the song control nucleus area X of the medial striatum in male zebra finches (Taeniopygia guttata). J. Comp. Neurol. 502 (2007) 544-562
Casto J.M., and Ball G.F. Characterization and localization of D1 dopamine receptors in the sexually dimorphic vocal control nucleus, area X, and the basal ganglia of European starlings. J. Neurobiol. 25 (1994) 767-780
Casto J.M., and Ball G.F. Early administration of 17β-estradiol partially masculinizes song control regions and a2-adrenergic receptor distribution in European starlings (Sturnus vulgaris). Horm. Behav. 30 (1996) 387-406
Civelli O., Bunzow J.R., and Grandy D.K. Molecular diversity of the dopamine receptors. Annu. Rev. Pharmacol. Toxicol. 32 (1993) 281-307
Clarke R.W., and Harris J. RX 821002 as tool for physiological investigation of alpha2-adrenoreceptors. CNS Drug Rev. 8 (2002) 177-193
Cooper J.R., Bloom F.E., and Roth R.H. Dopamine. In: Cooper J.R., Bloom F.E., and Roth R.H. (Eds). The Biochemical Basis of Neuropharmacology. eighth ed. (2003), Oxford University Press, New York 225-270
Cooper J.R., Bloom F.E., and Roth R.H. Norepinephrine and epinephrine. In: Cooper J.R., Bloom F.E., and Roth R.H. (Eds). The Biochemical Basis of Neuropharmacology. eighth ed. (2003), Oxford University Press, New York 181-224
Cornil C.A., Balthazart J., Motte P., Massotte L., and Seutin V. Dopamine activates noradrenergic receptors in the preoptic area. J. Neurosci. 22 (2002) 9320-9330
Dermon C.R., and Kouvelas E.D. Quantitative analysis of the localization of adrenergic binding sites in chick brain. J. Neurosci. Res. 23 (1989) 297-303
Diez-Alarcia R., Pilar-Cuellar F., Paniagua M.A., Meana J.J., and Fernandez-Lopez A. Pharmacological characterization and autoradiographic distribution of alpha2-adrenoceptor antagonist [3H]RX 821002 binding sites in the chicken brain. Neuroscience 141 (2006) 357-369
Ding L., and Perkel D.J. Dopamine modulates excitability of spiny neurons in the avian basal ganglia. J. Neurosci. 22 (2002) 5210-5218
Ding L., Perkel D.J., and Farries M.A. Presynaptic depression of glutamatergic synaptic transmission by D1-like dopamine receptor activation in the avian basal ganglia. J. Neurosci. 23 (2003) 6086-6095
Docherty J.R. Subtypes of functional alpha1- and alpha2-adrenoceptors. Eur. J. Pharmacol. 361 (1998) 1-15
Dudley M.W., Howard B.D., and Cho A.K. The interaction of the betahaloethyl benzylamines, xylamine, and DSP-4 with catecholaminergic neurons. Annu. Rev. Pharmacol. Toxicol. 30 (1990) 387-403
Fritschy J.M., and Grzanna R. Selective effects of DSP-4 on locus coeruleus axons: are there pharmacologically different types of noradrenergic axons in the central nervous system?. Prog. Brain Res. 88 (1991) 257-268
Gale S.D., and Perkel D.J. Properties of dopamine release and uptake in the songbird basal ganglia. J. Neurophysiol. 93 (2005) 1871-1879
Gibson A., and Samini M. The effects of bromocriptine on pre-synaptic and post-synaptic alpha-adrenoceptors in the mouse vas deferens. J. Pharm. Pharmacol. 31 (1979) 826-830
Greenberg D.A., U'Prichard D.C., and Snyder S.H. Alpha-noradrenergic binding in mammalian brain: differential labeling of agonist and antagonist states. Life Sci. 19 (1976) 69-76
Gresch P.J., Sved A.F., Zigmond M.J., and Finlay J.M. Local influence of endogenous norepinephrine on extracellular dopamine in rat medial prefrontal cortex. J. Neurochem. 65 (1995) 111-116
Hallman H., Sundstrom E., and Jonsson G. Effects of the noradrenaline neurotoxin DSP 4 on monoamine neurons and their transmitter turnover in rat CNS. J. Neural Transm. 60 (1984) 89-102
Halme M., Sjoholm B., and Scheinin M. Recombinant human a2-adrenoceptor subtypes: comparison of [3H]rauwolscine, [3H]atipamezole and [3H]RX821002 as radioligands. Biochim. Biophys. Acta 1266 (1995) 207-214
Hara E., Kubikova L., Hessler N.A., and Jarvis E.D. Role of the midbrain dopaminergic system in modulation of vocal brain activation by social context. Eur. J. Neurosci. 25 (2007) 3406-3416
Harrison J.K., D'Angelo D.D., Zeng D.W., and Lynch K.R. Pharmacological characterization of rat alpha 2-adrenergic receptors. Mol. Pharmacol. 40 (1991) 407-412
Harrison J.K., Pearson W.R., and Lynch K.R. Molecular characterization of alpha1- and alpha2-adrenoreceptors. TINS 12 (1991) 62-67
Heimovics S.A., and Riters L.V. Immediate early gene activity in song control nuclei and brain areas regulating motivation relates positively to singing behavior during, but not outside of, a breeding context. J. Neurobiol. 65 (2005) 207-224
Hessler N.A., and Doupe A.J. Social context modulates singing-related neural activity in the songbird forebrain. Nat. Neurosci. 2 (1999) 209-211
Hoffman B.B., and Lefkowitz R.J. Catecholamines, sympathomimetic drugs and adrenergic receptor antagonists. In: Hardman J.G., Goodman Gilman A., and Limbird L.E. (Eds). The Pharmacological Basis of Therapeutics. ninth ed. (1996), The McGraw-Hill Companies 199-248
Izenwasser S., Werling L.L., and Cox B.M. Comparison of the effects of cocaine and other inhibitors of dopamine uptake in rat striatum, nucleus accumbens, olfactory tubercle, and medial prefrontal cortex. Brain Res. 520 (1990) 303-309
Jaber M., Robinson S.W., Missale C., and Caron M.G. Dopamine receptors and brain function. Neuropharmacology 35 (1996) 1503-1519
Jaim-Etcheverry G., and Zieher L.M. DSP-4: a novel compound with neurotoxic effects on noradrenergic neurons of adult and developing rats. Brain Res. 188 (1980) 513-523
Jarvis E.D., Scharff C., Grossman M.R., Ramos J.A., and Nottebohm F. For whom the bird sings: context-dependent gene expression. Neuron 21 (1998) 775-788
Johnson F., Sablan M.M., and Bottjer S.W. Topographic organization of a forebrain pathway involved with vocal learning in zebra finches. J. Comp. Neurol. 358 (1995) 260-278
Johnston A.L., and File S.E. Yohimbine's anxiogenic action: evidence for noradrenergic and dopaminergic sites. Pharmacol. Biochem. Behav. 32 (1989) 151-156
Kao M.H., and Brainard M.S. Lesions of an avian basal ganglia circuit prevent context-dependent changes to song variability. J. Neurophysiol. 96 (2006) 1441-1455
Kao M.H., Doupe A.J., and Brainard M.S. Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 433 (2005) 638-643
Konishi M. The role of auditory feedback in birdsong. Ann. N. Y. Acad. Sci. 1016 (2004) 463-475
Kroodsma D.E., and Konishi M. A suboscine bird (eastern phoebe Sayornis phoebe) develops normal song without auditory feedback. Anim. Behav. 42 (1991) 477-487
Kuhar M.J., Minneman K., and Muly E.C. Catecholamines. In: Siegel G., Albers R.W., Brady S., and Price D. (Eds). Basic Neurochemistry. seventh ed. (2006), Elsevier Academic Press 211-226
Lanau F., Zenner M.T., Civelli O., and Hartman D.S. Epinephrine and norepinephrine act as potent agonists at the recombinant human dopamine D4 receptor. J. Neurochem. 68 (1997) 804-812
Lewis J.W., Ryan S.M., Arnold A.P., and Butcher L.L. Evidence for a catecholaminergic projection to area X in the zebra finch. J. Comp. Neurol. 196 (1981) 347-354
Malenka R.C., and Nicoll R.A. Dopamine decreases in the calcium-activated afterhyperpolarization in hippocampal CA1 pyramidal cells. Brain Res. 379 (1986) 210-215
Maney D.L., and Ball G.F. Fos-like immunoreactivity in catecholaminergic brain nuclei after territorial behavior in free-living song sparrows. J. Neurobiol. 56 (2003) 163-170
Mello C.V., Pinaud R., and Ribeiro S. Noradrenergic system of the zebra finch brain: immunocytochemical study of dopamine-beta-hydroxylase. J. Comp. Neurol. 400 (1998) 207-228
Missale C., Nash S.R., Robinson S.W., Jaber M., and Caron M.G. Dopamine receptors: from structure to function. Physiol. Rev. 78 (1998) 189-225
Misu Y., Goshima Y., Ueda H., and Kubo T. Presynaptic inhibitory dopamine receptors on noradrenergic nerve terminals: analysis of biphasic actions of dopamine and apomorphine on the release of endogenous norepinephrine in rat hypothalamic slices. J. Pharmacol. Exp. Ther. 235 (1985) 3
Moron J.A., Brockington A., Wise R.A., Rocha B.A., and Hope B.T. Dopamine uptake through norepinephrine transporter in brain regions with low levels of the dopamine trnasporter: evidence from knock out mouse lines. J. Neurosci. 22 (2002) 389-395
Newman-Tancredi A., Audinot-Bouchez V., Gobert A., and Millan M.J. Noradrenaline and adrenaline are high affinity agonists at dopamine D4 receptors. Eur. J. Pharmacol. 319 (1997) 379-383
Newman-Tancredi A., Nicolas J.P., Audinot V., Gavaudan S., Verriele L., Touzard M., Chaput C., Richard N., and Millan M.J. Actions of alpha2 adrenoceptor ligands at alpha2A and 5-HT1A receptors: the antagonist, atipamezole, and the agonist, dexmedetomidine, are highly selective for alpha2A adrenoceptors. Naunyn Schmiedebergs Arch. Pharmacol. 358 (1998) 197-206
Nock B., Johnson A.E., Feder H.H., and McEwen B.S. Tritium-sensitive film autoradiography of guinea pig brain alpha 2-noradrenergic receptors. Brain Res. 336 (1985) 148-152
Nottebohm F., Alvarez-Buylla A., Cynx J., Kirn J., Ling C.Y., Nottebohm M., Suter R., Tolles A., and Williams H. Song learning in birds: the relation between perception and production. Philos. Trans. R. Soc. Lond. B Biol. Sci. 329 (1990) 115-124
Nyronen T., Pihlavisto M., Peltonen J.M., Hoffren A.M., Varis M., Salminen T., Wurster S., Marjamaki A., Kanerva L., Katainen E., Laaksonen L., Savola J.M., Scheinin M., and Johnson M.S. Molecular mechanism for agonist-promoted alpha(2A)-adrenoceptor activation by norepinephrine and epinephrine. Mol. Pharmacol. 59 (2001) 1343-1354
O'Rourke M.F., Blaxall H.S., Iversen L.J., and Bylund D.B. Characterization of [3H]RX821002 binding to alpha-2 adrenergic receptor subtypes. J. Pharmacol. Exp. Ther. 268 (1994) 1362-1367
Pan W.H., Yang S.Y., and Lin S.K. Neurochemical interaction between dopaminergic and noradrenergic neurons in the medial prefrontal cortex. Synapse 53 (2004) 44-52
Perkel, D.J., Wendel, B.J., 2006. Dopamine-mediated effects on spontaneous firing rate in the songbird basal ganglia nucleus Area X. 2004 Abstract Viewer/Itinerary Planner. Society for Neuroscience, Atlanta, GE. Online Program No. 44.1.
Philipp M., Brede M., and Hein L. Physiological significance of a2-adrenergic receptor subtype diversity: one receptor is not enough. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283 (2002) R287-R295
Revilla V., Revilla R., and Fernandez-Lopez A. A comparative study of the beta-adrenoceptors in higher song nuclei of birds. Neurosci. Lett. 271 (1999) 9-12
Rey E., Hernandez-Diaz F.J., Abreu P., Alonso R., and Tabares L. Dopamine induces intracellular Ca2+ signals mediated by a1B-adrenoceptors in rat pineal cells. Eur. J. Pharmacol. 430 (2001) 9-17
Riters L.V., and Ball G.F. Sex differences in the densities of alpha2-adrenergic receptors in the song control system, but not the medial preoptic nucleus in zebra finches. J. Chem. Neuroanat. 23 (2002) 269-277
Riters L.V., Eens M., Pinxten R., and Ball G.F. Seasonal changes in the densities of alpha2-noradrenergic receptors are inversely related to changes in testosterone and the volumes of song control nuclei in male European starlings. J. Comp. Neurol. 444 (2002) 63-74
Robbins T.W., and Everitt B.J. Neurobehavioural mechanisms of reward and motivation. Curr. Opin. Neurobiol. 6 (1996) 228-236
Ruffolo R.R.J., Nichols A.J., Stadel J.M., and Hieble J.P. Pharmacologic and therapeutic applications of alpha2-adrenoceptor subtypes. Annu. Rev. Pharmacol. Toxicol. 32 (1993) 243-279
Ruuskanen J.O., Laurila J., Xhaard H., Rantanen V.-V., Vuoriluoto K., Wurster S., Marjamaki A., Vainio M., Johnson M.S., and Scheinin M. Conserved structural, pharmacological and functional properties among the three human and zebrafish a2-adrenoceptors. Br. J. Pharmacol. 144 (2005) 165-177
Scatton B., Zivkovic B., and Dedek J. Antidopaminergic properties of yohimbine. J. Pharm. Exp. Ther. 215 (1980) 494-499
Smeets W.J., and Gonzalez A. Catecholamine systems in the brain of vertebrates: new perspectives through a comparative approach. Brain Res. Brain Res. Rev. 33 (2000) 308-379
Starke K. Presynaptic autoreceptor in the third decade: focus on alpha2-adrenoceptors. J. Neurochem. 78 (2001) 685-693
Stokes T.M., Leonard C.M., and Nottebohm F. The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J. Comp. Neurol. 156 (1974) 337-374
Talley E.M., Rosin D.L., Lee A., Guyenet P.G., and Lynch K.R. Distribution of alpha 2A-adrenergic receptor-like immunoreactivity in the rat central nervous system. J. Comp. Neurol. 372 (1996) 111-134
Ueda H., Goshima Y., and Misu Y. Presynaptic alpha 2- and dopamine-receptor-mediated inhibitory mechanisms and dopamine nerve terminals in the rat hypothalamus. Neurosci. Lett. 40 (1983) 157-162
Unnerstall J.R., Kopajtic T.A., and Kuhar M.J. Distribution of α2 agonist binding sites in the rat and human central nervous system: analysis of some functional, anatomic correlates of the pharmacologic effects of clonidine and related adrenergic agents. Brain Res. Rev. 7 (1984) 69-101
Valentini V., Frau R., and Di Chiara G. Noradrenaline transporter blockers raise extracellular dopamine in medial prefrontal but not parietal and occipital cortex: differences with mianserin and clozapine. J. Neurochem. 88 (2004) 917-927
Williams H., and Mehta N. Changes in adult zebra finch song require a forebrain nucleus that is not necessary for song production. J. Neurobiol. 39 (1999) 14-28
Xu K., Naveri L., Frerichs K.U., Hallenbeck J.M., Feuerstein G., Davis J.N., and Siren A.L. Extracellular catecholamine levels in rat hippocampus after a selective alpha-2 adrenoceptor antagonist or a selective dopamine uptake inhibitor: evidence for dopamine release from local dopaminergic nerve terminals. J. Pharmacol. Exp. Ther. 267 (1993) 211-217
Young III W.S., and Kuhar M.J. A new method for receptor autoradiography: [3H]opioid receptors in rat brain. Brain Res. 179 (1979) 255-270
Zann R.A. Zebra Finch: A Synthesis of Laboratory and Field Studies (1996), Oxford University Press, New York
Zhang W., Klimek V., Farley J.T., Zhu M.-Y., and Ordway G.A. Alpha2C adrenoreceptors inhibit adenylyl cyclase in mouse striatum: potential activation by dopamine. J. Pharmacol. Exp. Ther. 289 (1999) 1286-1292
Zhang W.-P., Ouyang M., and Thomas S.A. Potency of catecholamines and other l-tyrosine derivatives at the cloned mouse adrenergic receptors. Neuropharmacology 47 (2004) 438-449