D1-like dopamine receptor density in nuclei involved in social behavior correlates with song in a context-dependent fashion in male European starlings.
Heimovics, Sarah A.; Cornil, Charlotte; Ball, Gregory F.et al.
[en] Research in songbirds shows that singing behavior is regulated by both brain areas involved in vocal behavior as well as those involved in social behavior. Interestingly, the precise role of these regions in song can vary as a function of the social, environmental and breeding context. To date, little is known about the neurotransmitters underlying such context-dependent regulation of song. Dopamine (DA) modulates highly motivated, goal-directed behaviors (including sexually motivated song) and emerging data implicate DA in the context-dependent regulation of singing behavior. This study was performed to begin to examine whether differences in DA receptors may underlie, in part, context-dependent differences in song production. We used autoradiographic procedures to label D1-like and D2-like DA receptors to examine the relationship between DA receptor density and singing behavior in multiple contexts in male European starlings (Sturnus vulgaris). Within a breeding context (when testosterone (T) was high), D1-like receptor density in the medial preoptic nucleus (POM) and midbrain central gray (GCt) negatively correlated with song used to attract a female. Additionally in this context, D1-like receptor density in POM, GCt, medial bed nucleus of the stria terminalis (BSTm), and lateral septum (LS) negatively correlated with song likely used to defend a nest box. In contrast, in a non-breeding context (when T was low), D1-like receptor density in POM and LS positively correlated with song used to maintain social flocks. No relationships were identified between song in any context and D2-like receptor densities. Differences in the brain regions and directional relationships between D1-like receptor binding and song suggest that dopaminergic systems play a region and context-specific role in song. These data also suggest that individual variation in singing behavior may, in part, be explained by individual differences in D1-like receptor density in brain regions implicated in social behavior.
Disciplines :
Neurosciences & behavior
Author, co-author :
Heimovics, Sarah A.; University of British Columbia - UBC > Department of Psychology / University of Wisconsin–Madison > Department of Zoology
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Ball, Gregory F.
Riters, Lauren V.
Language :
English
Title :
D1-like dopamine receptor density in nuclei involved in social behavior correlates with song in a context-dependent fashion in male European starlings.
Publication date :
2009
Journal title :
Neuroscience
ISSN :
0306-4522
eISSN :
1873-7544
Publisher :
Elsevier Science, New York, United States - New York
Absil P., Foidart A., Hemmings Jr. H.C., Steinbusch H.W., Ball G.F., and Balthazart J. Distribution of DARPP-32 immunoreactive structures in the quail brain: anatomical relationship with dopamine and aromatase. J Chem Neuroanat 21 (2001) 23-39
Adams D.B. Brain mechanisms of aggressive behavior: an updated review. Neurosci Biobehav Rev 30 (2006) 304-318
Alger S.J., and Riters L.V. Lesions to the medial preoptic nucleus differentially affect singing and nest box-directed behaviors within and outside of the breeding season in European starlings (Sturnus vulgaris). Behav Neurosci 120 (2006) 1326-1336
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 origin of catecholaminergic inputs to the song control nucleus RA in canaries. Neuroreport 13 (2002) 649-653
Appeltants D., Ball G.F., and Balthazart J. Song activation by testosterone is associated with an increased catecholaminergic innervation of the song control system in female canaries. Neuroscience 121 (2003) 801-814
Bailhache T., and Balthazart J. The catecholaminergic system of the quail brain: immunocytochemical studies of dopamine beta-hydroxylase and tyrosine hydroxylase. J Comp Neurol 329 (1993) 230-256
Ball G.F., and Balthazart J. Hormonal regulation of brain circuits mediating male sexual behavior in birds. Physiol Behav 83 (2004) 329-346
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., Riters L.V., and Balthazart J. Neuroendocrinology of song behavior and avian brain plasticity: multiple sites of action of sex steroid hormones. Front Neuroendocrinol 23 (2002) 137-178
Ball G.F., and Wingfield J.C. Changes in plasma-levels of luteinizing-hormone and sex steroid-hormones in relation to multiple-broodedness and nest-site density in male starlings. Physiol Zool 60 (1987) 191-199
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
Berridge K.C., and Robinson T.E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain Res Brain Res Rev 28 (1998) 309-369
Bharati I.S., and Goodson J.L. Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches. Neuroscience 143 (2006) 661-670
Blackburn J.R., Pfaus J.G., and Phillips A.G. Dopamine functions in appetitive and defensive behaviours. Prog Neurobiol 39 (1992) 247-279
Bottjer S.W. The distribution of tyrosine hydroxylase immunoreactivity in the brains of male and female zebra finches. J Neurobiol 24 (1993) 51-69
Brenowitz E.A., Margoliash D., and Nordeen K.W. An introduction to birdsong and the avian song system. J Neurobiol 33 (1997) 495-500
Burgdorf J., Knutson B., Panksepp J., and Ikemoto S. Nucleus accumbens amphetamine microinjections unconditionally elicit 50-kHz ultrasonic vocalizations in rats. Behav Neurosci 115 (2001) 940-944
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
Charlier T.D., Ball G.F., and Balthazart J. Sexual behavior activates the expression of the immediate early genes c-fos and Zenk (egr-1) in catecholaminergic neurons of male Japanese quail. Neuroscience 131 (2005) 13-30
Chen F., and Lawrence A.J. The effects of antidepressant treatment on serotonergic and dopaminergic systems in fawn-hooded rats: a quantitative autoradiography study. Brain Res 976 (2003) 22-29
Cooper J.R., Bloom F.E., and Roth R.H. The biochemical basis of neuropharmacology (2003), Oxford University Press, New York
Cuthill I., and Hindmarsh A.M. Increase in starling song activity with removal of mate. Anim Behav 33 (1985) 326-328
Dawson A., King V.M., Bentley G.E., and Ball G.F. Photoperiodic control of seasonality in birds. J Biol Rhythms 16 (2001) 365-380
Eens M. Understanding the complex song of the European starling: an integrated approach. Adv Study Behav 26 (1997) 355-434
Eens M., and Pinxten R. Extra-pair courtship in the starling Sturnus-vulgaris. Ibis 132 (1990) 618-619
Eens M., Pinxten R., and Verheyen R.F. Function of the song and song repertoire in the European starling (Sturnus vulgaris): an aviary experiment. Behaviour 125 (1993) 51-66
Eens M., Pinxten R., and Verheyen R.F. Variation in singing activity during the breeding cycle of the European starling Sturnus vulgaris. Belg J Zool 124 (1994) 167-174
Feare C. The starling (1984), Oxford University Press, New York
Feldman R.S., Meyer J.S., and Quenzer L.F. Principles of neuropsychopharmacology (1997), Sinauer Associates, Sunderland, MA
Ferrari P.F., van Erp A.M., Tornatzky W., and Miczek K.A. Accumbal dopamine and serotonin in anticipation of the next aggressive episode in rats. Eur J Neurosci 17 (2003) 371-378
Goodson J.L. Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm Behav 34 (1998) 67-77
Goodson J.L. The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 48 (2005) 11-22
Goodson J.L., Eibach R., Sakata J., and Adkins-Regan E. Effect of septal lesions on male song and aggression in the colonial zebra finch (Taeniopygia guttata) and the territorial field sparrow (Spizella pusilla). Behav Brain Res 101 (1999) 167-180
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
Hausberger M., Richardyris M.A., Henry L., Lepage L., and Schmidt I. Song sharing reflects the social-organization in a captive group of European starlings (Sturnus-vulgaris). J Comp Psych 109 (1995) 222-241
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
Heimovics S.A., and Riters L.V. Breeding-context-dependent relationships between song and cFos labeling within social behavior brain regions in male European starlings (Sturnus vulgaris). Horm Behav 50 (2006) 726-735
Heimovics S.A., and Riters L.V. ZENK labeling within social behavior brain regions reveals breeding context-dependent patterns of neural activity associated with song in male European starlings (Sturnus vulgaris). Behav Brain Res 176 (2007) 333-343
Heimovics S.A., and Riters L.V. Evidence that dopamine within motivation and song control brain regions regulates birdsong context-dependently. Physiol Behav 95 (2008) 258-266
Hessler N.A., and Doupe A.J. Social context modulates singing-related neural activity in the songbird forebrain. Nat Neurosci 2 (1999) 209-211
Huang Y.C., and Hessler N.A. Social modulation during songbird courtship potentiates midbrain dopaminergic neurons. PLoS ONE 3 (2008) e3281
Hull E.M., Du J., Lorrain D.S., and Matuszewich L. Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation. J Neurosci 15 (1995) 7465-7471
Hull E.M., Du J., Lorrain D.S., and Matuszewich L. Testosterone, preoptic dopamine, and copulation in male rats. Brain Res Bull 44 (1997) 327-333
Irvin R.W., Szot P., Dorsa D.M., Potegal M., and Ferris C.F. Vasopressin in the septal area of the golden hamster controls scent marking and grooming. Physiol Behav 48 (1990) 693-699
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
Jasnow A.M., Davis M., and Huhman K.L. Involvement of central amygdalar and bed nucleus of the stria terminalis corticotropin-releasing factor in behavioral responses to social defeat. Behav Neurosci 118 (2004) 1052-1061
Kollack-Walker S., and Newman S.W. Mating and agonistic behavior produce different patterns of Fos immunolabeling in the male Syrian hamster brain. Neuroscience 66 (1995) 721-736
Korzan W.J., Forster G.L., Watt M.J., and Summers C.H. Dopaminergic activity modulation via aggression, status, and a visual social signal. Behav Neurosci 120 (2006) 93-102
Korzan W.J., Summers T.R., and Summers C.H. Manipulation of visual sympathetic sign stimulus modifies social status and plasma catecholamines. Gen Comp Endocrinol 128 (2002) 153-161
Lehner P.N. Handbook of ethological methods (1996), Cambridge University Press, Cambridge
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
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
Maney D.L., Bernard D.J., and Ball G.F. Gonadal steroid receptor mRNA in catecholaminergic nuclei of the canary brainstem. Neurosci Lett 311 (2001) 189-192
Maney D.L., Erwin K.L., and Goode C.T. Neuroendocrine correlates of behavioral polymorphism in white-throated sparrows. Horm Behav 48 (2005) 196-206
Margoliash D. Functional organization of forebrain pathways for song production and perception. J Neurobiol 33 (1997) 671-693
Mello C.V. Mapping vocal communication pathways in birds with inducible gene expression. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 188 (2002) 943-959
Miczek K.A., and Tornatzky W. Ethopharmacology of aggression: impact on autonomic and mesocorticolimbic activity. Ann N Y Acad Sci 794 (1996) 60-77
Moses J., Loucks J.A., Watson H.L., Matuszewich L., and Hull E.M. Dopaminergic drugs in the medial preoptic area and nucleus accumbens: effects on motor activity, sexual motivation, and sexual performance. Pharmacol Biochem Behav 51 (1995) 681-686
Mountjoy D.J., and Lemon R.E. Song as an attractant for male and female European starlings, and the influence of song complexity on their response. Behav Ecol Sociobiol 28 (1991) 97-100
Neisewander J.L., Lucki I., and McGonigle P. Behavioral and neurochemical effects of chronic administration of reserpine and SKF-38393 in rats. J Pharmacol Exp Ther 257 (1991) 850-860
Newman S.W. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann N Y Acad Sci 877 (1999) 242-257
Pfaus J.G., and Phillips A.G. Role of dopamine in anticipatory and consummatory aspects of sexual behavior in the male rat. Behav Neurosci 105 (1991) 727-743
Pinxten R., and Eens M. Polygyny in the European starling-effect on female reproductive success. Anim Behav 40 (1990) 1035-1047
Putnam S.K., Du J., Sato S., and Hull E.M. Testosterone restoration of copulatory behavior correlates with medial preoptic dopamine release in castrated male rats. Horm Behav 39 (2001) 216-224
Rauceo S., Harding C.F., Maldonado A., Gaysinkaya L., Tulloch I., and Rodriguez E. Dopaminergic modulation of reproductive behavior and activity in male zebra finches. Behav Brain Res 187 1 (2008) 133-139
Riters L.V., and Alger S.J. Neuroanatomical evidence for indirect connections between the medial preoptic nucleus and the song control system: possible neural substrates for sexually motivated song. Cell Tissue Res 316 (2004) 35-44
Riters L.V., and Ball G.F. Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris). Horm Behav 36 (1999) 276-286
Riters L.V., Eens M., Pinxten R., and Ball G.F. Seasonal changes in the densities of alpha(2)-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
Riters L.V., Eens M., Pinxten R., Duffy D.L., Balthazart J., and Ball G.F. Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm Behav 38 (2000) 250-261
Riters L.V., Schroeder M.B., Auger C.J., Eens M., Pinxten R., and Ball G.F. Evidence for opioid involvement in the regulation of song production in male European starlings (Sturnus vulgaris). Behav Neurosci 119 (2005) 245-255
Riters L.V., Teague D.P., Schroeder M.B., and Cummings S.E. Vocal production in different social contexts relates to variation in immediate early gene immunoreactivity within and outside of the song control system. Behav Brain Res 155 (2004) 307-318
Riters L.V., Teague D.P., Schroeder M.B., and Cummings S.E. Vocal production in different social contexts relates to variation in immediate early gene immunoreactivity within and outside of the song control system. Behav Brain Res 155 (2004) 307-318
Sakaguchi H., and Saito N. The acetylcholine and catecholamine contents in song control nuclei of zebra finch during song ontogeny. Brain Res Dev Brain Res 47 (1989) 313-317
Salamone J.D., Correa M., Mingote S., and Weber S.M. Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse. J Pharmacol Exp Ther 305 (2003) 1-8
Sasaki A., Sotnikova T.D., Gainetdinov R.R., and Jarvis E.D. Social context-dependent singing-regulated dopamine. J Neurosci 26 (2006) 9010-9014
Schnell S.A., You S., and El Halawani M.E. D1 and D2 dopamine receptor messenger ribonucleic acid in brain and pituitary during the reproductive cycle of the turkey hen. Biol Reprod 60 (1999) 1378-1383
Schroeder M.B., and Riters L.V. Pharmacological manipulations of dopamine and opioids have differential effects on sexually motivated song in male European starlings. Physiol Behav 88 (2006) 575-584
Schulz K.M., Richardson H.N., Romeo R.D., Morris J.A., Lookingland K.J., and Sisk C.L. Medial preoptic area dopaminergic responses to female pheromones develop during puberty in the male Syrian hamster. Brain Res 988 (2003) 139-145
Soha J.A., Shimizu T., and Doupe A.J. Development of the catecholaminergic innervation of the song system of the male zebra finch. J Neurobiol 29 (1996) 473-489
Summers R.W., Westlake G.E., and Feare C.J. Differences in the ages, sexes and physical condition of starlings Sturnus-vulgaris at the center and periphery of roosts. Ibis 129 (1987) 96-102
van Furth W.R., Wolterink G., and van Ree J.M. Regulation of masculine sexual behavior: involvement of brain opioids and dopamine. Brain Res Brain Res Rev 21 (1995) 162-184
Wang Z., Young L.J., Liu Y., and Insel T.R. Species differences in vasopressin receptor binding are evident early in development: comparative anatomic studies in prairie and montane voles. J Comp Neurol 378 (1997) 535-546
Wild J.M. Neural pathways for the control of birdsong production. J Neurobiol 33 (1997) 653-670
Wintink A.J., and Brudzynski S.M. The related roles of dopamine and glutamate in the initiation of 50-kHz ultrasonic calls in adult rats. Pharmacol Biochem Behav 70 (2001) 317-323
Wise R.A. Forebrain substrates of reward and motivation. J Comp Neurol 493 (2005) 115-121
Wommack J.C., and Delville Y. Chronic social stress during puberty enhances tyrosine hydroxylase immunoreactivity within the limbic system in golden hamsters. Brain Res 933 (2002) 139-143
Yanagihara S., and Hessler N.A. Modulation of singing-related activity in the songbird ventral tegmental area by social context. Eur J Neurosci 24 (2006) 3619-3627