Dopamine receptors in a songbird brain

Abstract

Dopamine is a key neuromodulatory transmitter in the brain. It acts through dopamine receptors to affect changes in neural activity, gene expression, and behavior. In songbirds, dopamine is released into the striatal song nucleus Area X, and the levels depend on social contexts of undirected and directed singing. This differential release is associated with differential expression of activity-dependent genes, such as egr1 (avian zenk), which in mammalian brain are modulated by dopamine receptors. Here we cloned from zebra finch brain cDNAs of all avian dopamine receptors: the D1 (D1A, D1B, D1D) and D2 (D2, D3, D4) families. Comparative sequence analyses of predicted proteins revealed expected phylogenetic relationships, in which the D1 family exists as single exon and the D2 family exists as spliced exon genes. In both zebra finch and chicken, the D1A, D1B, and D2 receptors were highly expressed in the striatum, the D1D and D3 throughout the pallium and within the mesopallium, respectively, and the D4 mainly in the cerebellum. Furthermore, within the zebra finch, all receptors, except for D4, showed differential expression in song nuclei relative to the surrounding regions and developmentally regulated expression that decreased for most receptors during the sensory acquisition and sensorimotor phases of song learning. Within Area X, half of the cells expressed both D1A and D2 receptors, and a higher proportion of the D1A-only-containing neurons expressed egr1 during undirected but not during directed singing. Our findings are consistent with hypotheses that dopamine receptors may be involved in song development and social context-dependent behaviors. J. Comp. Neurol. 518:741–769, 2010. © 2009 Wiley-Liss, Inc.

Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns

“…All animals were laboratory raised except the hummingbirds, which were captured from wild populations in Santa Theresa, Espirito Santo, Brazil (sombre hummingbird and rufous-breasted hermit) and in Riverside, California (Anna's hummingbird) Feenders et al, 2008), and the garden warblers which were caught on Helgoland and around Oldenburg, Germany (Mouritsen et al, 2005). These wild-caught birds and some of the brain sections from the other species are from animals collected in our prior studies Wada et al, 2004;Mouritsen et al, 2005;Feenders et al, 2008;Horita et al, 2010Horita et al, , 2012Kubikova et al, 2010 Because sensory stimuli or behavioral performance are associated with changes in expression of activity-dependent genes in the associated brain circuits, to assess basal expression patterns we measured gene expression in the brains of animals that were in silent control conditions, either with lights off or on after an overnight period of silence. To examine stimulus and behaviorally regulated patterns of the activity-dependent genes (BDNF, EGR1, C-FOS, C-JUN, ARC, and DUSP1), we used brain sections from animals that had undergone controlled behavioral experiments in our prior studies.…”

“…Our approach was based on the hypothesis that similar brain areas should express similar gene sets. We included genes that have a wide range of functions and cellular locations, from inside the nucleus to the extracellular space, including 21 glutamate neurotransmitter receptors , five dopamine neuromodulatory receptors (Kubikova et al, 2010), the SEMA6A axon guidance receptor , cannabinoid receptor (Soderstrom et al, 2004), and retinoic acid orphan related receptor beta (ROR-β; this study); the NRN, BDNF, and SCUBE1 protein ligands (Wada et al, 2006;Lovell et al, 2008); the DLX6 (this study), FOXP1,FOXP2,ER81,LHX8,LHX9,NKX2.1,PAX6,EGR1, (Jarvis and Nottebohm, 1997;Kimpo and Doupe, 1997;Haesler et al, 2004;Jarvis et al, 2005;Abellan et al, 2009); the FKBP1A (this study), DUSP1 (a.k.a. map kinase phosphatase 1 [mkp1]), and PPAPDC1A enzymes Horita et al, 2010Horita et al, , 2012; and a diverse set of membrane and cytoplasmic genes, including ARPP16 (this study), TMEM100 (this study), ARC, CADPS2, and S100B (Wada et al, 2006;Lovell et al, 2008) (Table 1).…”

“…A third, but less acknowledged, hypothesis is that the different subdivisions of the anterior DVR as a field are homologous to both cortical and claustrum/amygdala cell types Molnar and Butler, 2002). To address these hypotheses, a number of elegant comparative and manipulation experiments have since been performed, but still with continued conflicting conclusions Medina and Abellan, 2009;Nomura et al, 2009;Uchida et al, 2010;Wang et al, 2010; Aboitiz, 2011;Butler et al, 2011;Kuenzel et al, 2011;Medina et al, 2011;Puelles, 2011;Tanaka et al, 2011;Atoji and Karim 2012;Dugas-Ford et al, 2012;Suzuki et al, 2012).Resolving these hypotheses, we believe, is in part hampered by yet another set of unanswered questions on our still limited understanding of overall avian brain organization.To address this issue, here we quantitatively analyzed telencephalic expression profiles of 46 constitutive and 6 activity-responsive genes (52 total; (Kubikova et al, 2010), the SEMA6A axon guidance receptor , cannabinoid receptor (Soderstrom et al, 2004), and retinoic acid orphan related receptor beta (ROR-β; this study); the NRN, BDNF, and SCUBE1 protein ligands (Wada et al, 2006;Lovell et al, 2008); the DLX6 (this study), FOXP1, FOXP2, ER81, COUP-TF2, LHX8, LHX9, NKX2.1, PAX6, EGR1, C-FOS, and C-JUN transcriptions factors (Jarvis and Nottebohm, 1997;Kimpo and Doupe, 1997;Haesler et al, 2004;Jarvis et al, 2005;Abellan et al, 2009); the FKBP1A (this study), DUSP1 (a.k.a. map kinase phosphatase 1 [mkp1]), and PPAPDC1A enzymes Horita et al, 2010Horita et al, , 2012; and a diverse set of membrane and cytoplasmic genes, including ARPP16 (this study), TMEM100 (this study), ARC, CADPS2, and S100B (Wada et al, 2006;Lovell et al, 2008) (Table 1).…”

Characterization of the Dopamine System in the Brain of the Túngara Frog, <i>Physalaemus pustulosus</i>

“…Importantly, every node in this network (which includes the preoptic area, anterior hypothalamus, ventromedial hypothalamus, medial amygdala and bed nucleus of the stria terminalis, periaqueductal grey/central grey, and the lateral septum) expresses dopamine D 1 receptors in every major vertebrate lineage studied to date [ mammals: Weiner et al, 1991;Savasta et al, 1986;Camps et al, 1990;Mansour et al, 1991;Jansson et al, 1999;Hurd et al, 2001;birds: Schnabel et al, 1997;Durstewitz et al, 1998;Sun et al, 2000;Absil et al, 2001;reptiles: Smeets et al, 2003reptiles: Smeets et al, , 2001; teleosts: Kapsimali et al, 2000;O'Connell et al, 2010b]. The only exception seems to be in the avian ventromedial hypothalamus, where presence of dopamine D 1 receptors has not been reported [Kubikova et al, 2010]. We have shown here that the dopaminoreceptive cells are present within each of these brain regions in P. pustulosus , suggesting that in amphibians dopamine plays as central a role in modulating social behavior as it does in other vertebrates.…”

Radioactive <em>in situ</em> Hybridization for Detecting Diverse Gene Expression Patterns in Tissue

“…Radioactive in situ hybridization of mRNA expression is widely used for multiple purposes, including for studying regional tissue organization, cell types, and brain functional activity [2][3][4][5]10,[12][13][14] . The later use is on genes whose mRNA expression in the brain is dependent on increased neural activity, often called activity-dependent genes or immediate early genes.…”