Top

Published in:

01-09-2009 | Original Article

Distribution of D₁ and D₅ dopamine receptors in the primate and rat basolateral amygdala

Authors: E. Chris Muly, Murat Senyuz, Zafar U. Khan, Ji-Dong Guo, Rimi Hazra, Donald G. Rainnie

Published in: Brain Structure and Function | Issue 4-5/2009

Abstract

Dopamine, acting at the D1 family receptors (D1R) is critical for the functioning of the amygdala, including fear conditioning and cue-induced reinstatement of drug self administration. However, little is known about the different contributions of the two D1R subtypes, D₁ and D₅. We identified D₁-immunoreactive patches in the primate that appear similar to the intercalated cell masses reported in the rodent; however, both receptors were present across the subdivisions of the primate amygdala including the basolateral amygdala (BLA). Using immunoelectron microscopy, we established that both receptors have widespread distributions in BLA. The D1R subtypes colocalize in dendritic spines and terminals, with D₁ predominant in spines and D₅ in terminals. Single-cell RT-PCR confirmed that individual BLA projection neurons express both D₁ and D₅ mRNA. The responses of primate BLA neurons to dopamine and D1R drugs were studied using in vitro slices. We found that responses were similar to those previously reported in rat BLA neurons and included a mixture of postsynaptic and presynaptic actions. We investigated the distribution of D1R in the rat BLA and found that there were similarities between the species, such as more prominent D₅ localization to presynaptic structures. The higher affinity of D₅ for dopamine suggests that presynaptic actions may predominate in the BLA at low levels of dopamine, while postsynaptic effects increase and dominate as dopaminergic drive increases. The results presented here suggest a complex action of dopamine on BLA circuitry that may evolve with different degrees of dopaminergic stimulation.

Berglind WJ, Case JM, Parker MP, Fuchs RA, See RE (2006) Dopamine D1 or D2 receptor antagonism within the basolateral amygdala differentially alters the acquisition of cocaine-cue associations necessary for cue-induced reinstatement of cocaine-seeking. Neuroscience 137:699–706PubMedCrossRef

Berretta S, Pantazopoulos H, Caldera M, Pantazopoulos P, Pare D (2005) Infralimbic cortex activation increases c-Fos expression in intercalated neurons of the amygdala. Neuroscience 132:943–953PubMedCrossRef

Bissiere S, Humeau Y, Luthi A (2003) Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition. Nat Neurosci 6:587–592PubMedCrossRef

Bordelon-Glausier JR, Khan ZU, Muly EC (2008) Quantification of D1 and D5 dopamine receptor localization in layers I, III, and V of Macaca mulatta prefrontal cortical area 9: coexpression in dendritic spines and axon terminals. J Comp Neurol 508:893–905PubMedCrossRef

Centonze D, Grande C, Saulle E, Martin AB, Gubellini P, Pavon N, Pisani A, Bernardi G, Moratalla R, Calabresi P (2003) Distinct roles of D1 and D5 dopamine receptors in motor activity and striatal synaptic plasticity. J Neurosci 23:8506–8512PubMed

Ciccocioppo R, Sanna PP, Weiss F (2001) Cocaine-predictive stimulus induces drug-seeking behavior and neural activation in limbic brain regions after multiple months of abstinence: reversal by D1 antagonists. Proc Natl Acad Sci 98:1976–1981PubMedCrossRef

Civelli O, Bunzow JB, Grandy DK (1993) Molecular diversity of the dopamine receptors. Ann Rev Pharmacol Toxicol 32:281–307CrossRef

de la Mora MP, Cardenas-Cachon L, Vazquez-Garcia M, Crespo-Ramirez M, Jacobsen K, Hoistad M, Agnati L, Fuxe K (2005) Anxiolytic effects of intra-amygdaloid injection of the D1 antagonist SCH23390 in the rat. Neurosci Lett 377:101–105CrossRef

Filip M, Thomas ML, Cunningham KA (2000) Dopamine D5 receptors in nucleus accumbens contribute to the detection of cocaine in rats. J Neurosci 20:RC98PubMed

Friedman E, Jin LQ, Cai GP, Hollon TR, Drago J, Sibley DR, Wang HY (1997) D₁-like dopaminergic activation of phosphoinositide hydrolysis is independent of D_1A dopamine receptors: evidence from D_1A knockout mice. Mol Pharmacol 51:6–11PubMed

Fuxe K, Jacobsen KX, Hoistad M, Tinner B, Jansson A, Staines WA, Agnati LF (2003) The dopamine D1 receptor-rich main and paracapsular intercalated nerve cell groups of the rat amygdala: relationship to the dopamine innervation. Neuroscience 119:733–746PubMedCrossRef

Ghashghaei HT, Barbas H (2002) Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115:1261–1279PubMedCrossRef

Gingrich JA, Caron MG (1993) Recent advances in the molecular biology of dopamine receptors. Annu Rev Neurosci 16:299–321PubMedCrossRef

Greba Q, Kokkinidis L (2000) Peripheral and intraamygdalar administration of the dopamine D1 receptor antagonist SCH 23390 blocks fear-potentiated startle but not shock reactivity or the shock sensitization of acoustic startle. Behav Neurosci 114:262–272PubMedCrossRef

Guarraci FA, Frohardt RJ, Kapp BS (1999) Amygdaloid D1 dopamine receptor involvement in Pavlovian fear conditioning. Brain Res 827:28–40PubMedCrossRef

Hersch SM, Ciliax BJ, Gutekunst C-A, Rees HD, Heilman CJ, Yung KKL, Bolam JP, Ince E, Yi H, Levey AI (1995) Electron microscopic analysis of D1 and D2 dopamine receptor proteins in the dorsal striatum and their synaptic relationships with motor corticostriatal afferents. J Neurosci 15:5222–5237PubMed

Hersi AI, Kitaichi K, Srivastava LK, Gaudreau P, Quirion R (2000) Dopamine D-5 receptor modulates hippocampal acetylcholine release. Brain Res Mol Brain Res 76:336–340PubMedCrossRef

Jacobsen KX, Hoistad M, Staines WA, Fuxe K (2006) The distribution of dopamine D1 receptor and mu-opioid receptor 1 receptor immunoreactivities in the amygdala and interstitial nucleus of the posterior limb of the anterior commissure: relationships to tyrosine hydroxylase and opioid peptide terminal systems. Neuroscience 141:2007–2018PubMedCrossRef

Jasnow AM, Daftary SS, Rainnie DG (2008) Modificaiton of spike timing precision and high threshold oscillations by inhibitory synaptic input in basolateral amygdala neurons. Program No.41.3.2008 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience

Khan ZU, Gutierrez A, Martin R, Penafiel A, Rivera A, de la CA (2000) Dopamine D5 receptors of rat and human brain. Neuroscience 100:689–699PubMedCrossRef

Kroner S, Rosenkranz JA, Grace AA, Barrionuevo G (2005) Dopamine modulates excitability of basolateral amygdala neurons in vitro. J Neurophysiol 93:1598–1610PubMedCrossRef

Kurimoto K, Yabuta Y, Ohinata Y, Ono Y, Uno KD, Yamada RG, Ueda HR, Saitou M (2006) An improved single-cell cDNA amplification method for efficient high-density oligonucleotide microarray analysis. Nucleic Acids Res 34:e42PubMedCrossRef

Lamont EW, Kokkinidis L (1998) Infusion of the dopamine D1 receptor antagonist SCH 23390 into the amygdala blocks fear expression in a potentiated startle paradigm. Brain Res 795:128–136PubMedCrossRef

Laplante F, Sibley DR, Quirion R (2004) Reduction in acetylcholine release in the hippocampus of dopamine D5 receptor-deficient mice. Neuropsychopharmacology 29:1620–1627PubMedCrossRef

Lee FJ, Xue S, Pei L, Vukusic B, Chery N, Wang Y, Wang YT, Niznik HB, Yu XM, Liu F (2002) Dual regulation of NMDA receptor functions by direct protein–protein interactions with the dopamine D1 receptor. Cell 111:219–230PubMedCrossRef

Lei W, Jiao Y, Del Mar N, Reiner A (2004) Evidence for differential cortical input to direct pathway versus indirect pathway striatal projection neurons in rats. J Neurosci 24:8289–8299PubMedCrossRef

Leonard SK, Anderson CM, Lachowicz JE, Schulz DW, Kilts CD, Mailman RB (2003) Amygdaloid D1 receptors are not linked to stimulation of adenylate cyclase. Syn 50:320–333CrossRef

Levita L, Mania I, Rainnie DG (2003) Dopamine activates multiple conductances in the basolateral amygdala. Society for Neuroscience Abstract Viewer and Itinerary Planner Program#336, p 19

Likhtik E, Pelletier JG, Paz R, Pare D (2005) Prefrontal control of the amygdala. J Neurosci 25:7429–7437PubMedCrossRef

Liu F, Wan Q, Pristupa ZB, Yu XM, Wang YT, Niznik HB (2000) Direct protein–protein coupling enables cross-talk between dopamine D5 and gamma-aminobutyric acid A receptors. Nature 403:274–280PubMedCrossRef

Loretan K, Bissiere S, Luthi A (2004) Dopaminergic modulation of spontaneous inhibitory network activity in the lateral amygdala. Neuropharmacology 47:631–639PubMedCrossRef

Macedo CE, Martinez RC, Albrechet-Souza L, Molina VA, Brandao ML (2007) 5-HT2- and D1-mechanisms of the basolateral nucleus of the amygdala enhance conditioned fear and impair unconditioned fear. Behav Brain Res 177:100–108PubMedCrossRef

Maltais S, te C, Drolet G, Falardeau P (2000) Cellular colocalization of dopamine D1 mRNA and D2 receptor in rat brain using a D2 dopamine receptor specific polyclonal antibody. Prog Neuropsychopharmacol Biol Psychiatry 24:1127–1149PubMedCrossRef

Mansour A, Meador-Woodruff JH, Zhou QY, Civelli O, Akil H, Watson SJ (1991) A comparison of D1 receptor binding and mRNA in rat brain using receptor autoradiographic and in situ hybridization techniques. Neuroscience 45:359–371PubMedCrossRef

Marowsky A, Yanagawa Y, Obata K, Vogt KE (2005) A specialized subclass of interneurons mediates dopaminergic facilitation of amygdala function. Neuron 48:1025–1037PubMedCrossRef

McDonald AJ, Mascagni F, Mania I, Rainnie DG (2005) Evidence for a perisomatic innervation of parvalbumin-containing interneurons by individual pyramidal cells in the basolateral amygdala. Brain Res 1035:32–40PubMedCrossRef

Mitrano DA, Smith Y (2007) Comparative analysis of the subcellular and subsynaptic localization of mGluR1a and mGluR5 metabotropic glutamate receptors in the shell and core of the nucleus accumbens in rat and monkey. J Comp Neurol 500:788–806PubMedCrossRef

Montague DM, Striplin CD, Overcash JS, Drago J, Lawler CP, Mailman RB (2001) Quantification of D1B(D5) receptors in dopamine D1A receptor-deficient mice. Syn 39:319–322CrossRef

Muly EC, Szigeti K, Goldman-Rakic PS (1998) D₁ receptor in interneurons of macaque prefrontal cortex: distribution and subcellular localization. J Neurosci 18:10553–10565PubMed

Muly EC, Greengard P, Goldman-Rakic PS (2001) Distribution of protein phosphatases-1α and -1γ1 and the D1 dopamine receptor in primate prefrontal cortex: evidence for discrete populations of spines. J Comp Neurol 440:261–270PubMedCrossRef

Muly EC, Maddox M, Smith Y (2003) Distribution of mGluR1α and mGluR5 immunolabeling in primate prefrontal cortex. J Comp Neurol 467:521–535PubMedCrossRef

Nader K, LeDoux JE (1999) Inhibition of the mesoamygdala dopaminergic pathway impairs the retrieval of conditioned fear associations. Behav Neurosci 113:891–901PubMedCrossRef

Pape HC, Pare D, Driesang RB (1998) Two types of intrinsic oscillations in neurons of the lateral and basolateral nuclei of the amygdala. J Neurophysiol 79:205–216PubMed

Paspalas CD, Goldman-Rakic PS (2004) Microdomains for dopamine volume neurotransmission in primate prefrontal cortex. J Neurosci 24:5292–5300PubMedCrossRef

Peters A, Palay SL, Webster HD (1991) The fine structure of the nervous system: neurons and their supporting cells. Oxford University Press, New York

Pickel VM, Colago EE, Mania I, Molosh AI, Rainnie DG (2006) Dopamine D1 receptors co-distribute with N-methyl-d-aspartic acid type-1 subunits and modulate synaptically-evoked N-methyl-d-aspartic acid currents in rat basolateral amygdala. Neuroscience 142:671–690PubMedCrossRef

Pinto A, Sesack SR (2008) Ultrastructural analysis of prefrontal cortical inputs to the rat amygdala: spatial relationships to presumed dopamine axons and D1 and D2 receptors. Brain Struct Funct 213:159–175PubMedCrossRef

Rainnie DG (1999) Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82:69–85PubMed

Rainnie DG, Ressler KJ (2009) Physiology of the Amygdala: implications for PTSD. In: Shiromani P, Keane T, LeDoux J (eds) Post-traumatic stress disorder: basic science and clinical practice. Humana Press, New York, pp 39–78

Rainnie DG, Asprodini EK, Shinnick-Gallagher P (1993) Intracellular recordings from morphologically identified neurons of the basolateral amygdala. J Neurophysiol 69:1350–1362PubMed

Rainnie DG, Bergeron R, Sajdyk TJ, Patil M, Gehlert DR, Shekhar A (2004) Corticotrophin releasing factor-induced synaptic plasticity in the amygdala translates stress into emotional disorders. J Neurosci 24:3471–3479PubMedCrossRef

Rainnie DG, Mania I, Mascagni F, McDonald AJ (2006) Physiological and morphological characterization of parvalbumin-containing interneurons of the rat basolateral amygdala. J Comp Neurol 498:142–161PubMedCrossRef

Rosenkranz JA, Grace AA (2001) Dopamine attenuates prefrontal cortical suppression of sensory inputs to the basolateral amygdala of rats. J Neurosci 21:4090–4103PubMed

Rosenkranz JA, Grace AA (2002) Cellular mechanisms of infralimbic and prelimbic prefrontal cortical inhibition and dopaminergic modulation of basolateral amygdala neurons in vivo. J Neurosci 22:324–337PubMed

Sah P, Faber ES, Lopez dA, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–834PubMed

Sahu A, Tyeryar KR, Vongtau HO, Sibley DR, Undieh AS (2008) D5 Dopamine receptors are required for dopaminergic activation of phospholipase C. Mol Pharmacol 75:447–453PubMedCrossRef

Scibilia RJ, Lachowicz JE, Kilts CD (1992) Topographic nonoverlapping distribution of D1 and D2 dopamine receptors in the amygdaloid nuclear complex of the rat brain. Syn 11:146–154CrossRef

See RE, Kruzich PJ, Grimm JW (2001) Dopamine, but not glutamate, receptor blockade in the basolateral amygdala attenuates conditioned reward in a rat model of relapse to cocaine-seeking behavior. Psychopharmacology (Berl) 154:301–310CrossRef

See RE, Fuchs RA, Ledford CC, McLaughlin J (2003) Drug addiction, relapse, and the amygdala. Ann N Y Acad Sci 985:294–307PubMedCrossRef

Smiley JF, Levey AI, Ciliax BJ, Goldman-Rakic PS (1994) D₁ dopamine receptor immunoreactivity in human and monkey cerebral cortex: predominant and extrasynaptic localization in dendritic spines. Proc Natl Acad Sci USA 91:5720–5724PubMedCrossRef

Sunahara RK, Guan H-C, O’Dowd BF, Seeman P, Laurier LG, Ng G, George SR, Torchia J, Van Tol HHM, Niznik HB (1991) Cloning of the gene for a human dopamine D₅ receptor with a higher affinity for dopamine than D₁. Nature 350:614–619PubMedCrossRef

Tiberi M, Jarvie KR, Silvia C, Falardeau P, Gingrich JA, Godinot N, Bertrand L, Yang-Feng TL, Fremeau RT Jr, Caron MG (1991) Cloning, molecular characterization, and chromosomal assignment of a gene encoding a second D1 dopamine receptor subtype: differential expression pattern in rat brain compared with the D1A receptor. Proc Natl Acad Sci USA 88:7491–7495PubMedCrossRef

Undie AS, Friedman E (1990) Stimulation of a dopamine D1 receptor enhances inositol phosphates formation in rat brain. J Pharmacol Exp Ther 253:987–992PubMed

Weinshank RL, Adham N, Macchi M, Olsen MA, Branchek TA, Hartig PR (1991) Molecular cloning and characterization of a high affinity dopamine receptor (D1 beta) and its pseudogene. J Biol Chem 266:22427–22435PubMed

Woodruff AR, Sah P (2007) Inhibition and synchronization of basal amygdala principal neuron spiking by parvalbumin-positive interneurons. J Neurophysiol 98:2956–2961PubMedCrossRef

Yamamoto R, Ueta Y, Kato N (2007) Dopamine induces a slow afterdepolarization in lateral amygdala neurons. J Neurophysiol 98:984–992PubMedCrossRef

Yokoyama M, Suzuki E, Sato T, Maruta S, Watanabe S, Miyaoka H (2005) Amygdalic levels of dopamine and serotonin rise upon exposure to conditioned fear stress without elevation of glutamate. Neurosci Lett 379:37–41PubMedCrossRef

Title: Distribution of D1 and D5 dopamine receptors in the primate and rat basolateral amygdala
Authors: E. Chris Muly
Murat Senyuz
Zafar U. Khan
Ji-Dong Guo
Rimi Hazra
Donald G. Rainnie
Publication date: 01-09-2009
Publisher: Springer-Verlag
Published in: Brain Structure and Function / Issue 4-5/2009
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-009-0214-8

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Distribution of D₁ and D₅ dopamine receptors in the primate and rat basolateral amygdala

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4-5/2009

Superior olivary complex organization and cytoarchitecture may be correlated with function and catarrhine primate phylogeny

Differential topography of the bilateral cortical projections to the whisker and forepaw regions in rat motor cortex

An fMRI case study of visual memory in a patient with epilepsy: comparison before and after temporal lobe surgery

The Neuroscience Peer Review Consortium

Left cytoarchitectonic area 44 supports selection in the mental lexicon during language production

Synaptic circuitry in the retinorecipient layers of the optic tectum of the lamprey (Lampetra fluviatilis). A combined hodological, GABA and glutamate immunocytochemical study