Home LiteratureArticle Details
PMID: 8922403 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses.

Otmakhova NA, Lisman JE

Abstract

The role of the mesolimbic dopaminergic system in the reinforcement of learning suggests that dopamine should be able to modulate activity-dependent synaptic plasticity. We have examined the effect of D1/D5 agonists on early long-term potentiation (LTP) (40 min) in the CA1 region of hippocampal slices. D1/D5 agonists (+)bromo-APB, 6-chloro-PB, and dihydrexidine increased the magnitude of LTP in a synapse-specific manner (by approximately 10, 15, and 20%, respectively). This D1/D5 effect was mimicked by a low dose (10 microM) of the adenylyl cyclase activator forskolin. The D1/D5 antagonist (+)SCH 23390 reduced early LTP. In catecholamine-depleted slices, LTP was smaller by approximately 20-25% and could not be decreased further by D1/D5 antagonist. Under these conditions, D1/D5 agonist 6-chloro-PB and forskolin produced a larger enhancement of LTP (20-25%), restoring it to the control level. At the same dose, dideoxyforskolin did not affect early LTP. The D1/D5 agonist effect was completely blocked by the D1/D5 antagonist (+)SCH 23390. These results indicate that dopamine produces a synapse-specific enhancement of early LTP through D1/D5 receptors and cAMP.

MeSH Terms
Animals Catecholamines/deficiency Colforsin/metabolism Dopamine Agonists/pharmacology Dopamine Antagonists/pharmacology Hippocampus/physiology Long-Term Potentiation/drug effects Rats Rats, Inbred Strains Receptors, Dopamine D1/physiology Receptors, Dopamine D5 Synapses/physiology
Chemicals
Catecholamines Dopamine Agonists Dopamine Antagonists Drd5 protein, rat Receptors, Dopamine D1 Receptors, Dopamine D5 Colforsin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Otmakhova N A
Department of Biology and Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02254, USA.
Lisman J E
References (72)
72 references, click to expand
  1. Dopamine decreases the calcium-activated afterhyperpolarization in hippocampal CA1 pyramidal cells.
    Brain Res. 1986 Aug 6;379(2):210-5 PMID: 3017510
  2. Multiple receptors for dopamine.
    Nature. 1979 Jan 11;277(5692):93-6 PMID: 215920
  3. Long-term increases in excitability in the CA1 region of rat hippocampus induced by beta-adrenergic stimulation: possible mediation by cAMP.
    J Neurosci. 1992 Feb;12(2):506-17 PMID: 1311033
  4. Modulation by dopamine of population responses and cell membrane properties of hippocampal CA1 neurons in vitro.
    Brain Res. 1984 Feb 6;292(2):327-38 PMID: 6318915
  5. Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain.
    J Neurosci. 1995 Dec;15(12):7821-36 PMID: 8613722
  6. Stimulation of both dopamine D1 and D2 receptors facilitates in vivo acetylcholine release in the hippocampus.
    Brain Res. 1993 Aug 6;618(2):341-5 PMID: 8104086
  7. Immunohistochemical localization of the D1 dopamine receptor in rat brain reveals its axonal transport, pre- and postsynaptic localization, and prevalence in the basal ganglia, limbic system, and thalamic reticular nucleus.
    Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11988-92 PMID: 1281547
  8. Selective expression of one Ca(2+)-inhibitable adenylyl cyclase in dopaminergically innervated rat brain regions.
    Brain Res Mol Brain Res. 1994 Mar;22(1-4):236-44 PMID: 8015383
  9. Inhibitory influence via 5-HT3 receptors on the induction of LTP in mossy fiber-CA3 system of guinea-pig hippocampal slices.
    Neurosci Res. 1994 Jan;18(4):277-82 PMID: 8190370
  10. Addictive drugs and brain stimulation reward.
    Annu Rev Neurosci. 1996;19:319-40 PMID: 8833446
  11. Modulation of synaptic efficacy in field CA1 of the rat hippocampus by forskolin.
    Brain Res. 1992 Mar 6;574(1-2):85-92 PMID: 1379110
  12. Dopamine changes the shape of action potentials in hippocampal pyramidal cells.
    Brain Res. 1985 Sep 9;342(2):386-90 PMID: 4041844
  13. The CaM kinase II hypothesis for the storage of synaptic memory.
    Trends Neurosci. 1994 Oct;17(10):406-12 PMID: 7530878
  14. Autoradiographic distribution of [3H]YM-09151-2, a high-affinity and selective antagonist ligand for the dopamine D2 receptor group, in the rat brain and spinal cord.
    J Comp Neurol. 1994 Jun 1;344(1):121-36 PMID: 7914895
  15. Association of protein kinase A and protein phosphatase 2B with a common anchoring protein.
    Science. 1995 Jan 6;267(5194):108-11 PMID: 7528941
  16. Dopaminergic modulation of dye coupling between neurons in the core and shell regions of the nucleus accumbens.
    J Neurosci. 1993 Aug;13(8):3456-71 PMID: 8340817
  17. Depletion of norepinephrine, but not serotonin, reduces long-term potentiation in the dentate gyrus of rat hippocampal slices.
    J Neurosci. 1985 Aug;5(8):2169-76 PMID: 4040556
  18. Heterogeneous tissue-specific transcription of dopamine receptor subtype messenger RNA in rat brain.
    Brain Res Mol Brain Res. 1994 Sep;25(3-4):344-50 PMID: 7808233
  19. Activation of dopamine D1 receptors enhances long-term depression of synaptic transmission induced by low frequency stimulation in rat hippocampal CA1 neurons.
    Neurosci Lett. 1995 Mar 31;188(3):195-8 PMID: 7609907
  20. Expression of a calmodulin-dependent phosphodiesterase isoform (PDE1B1) correlates with brain regions having extensive dopaminergic innervation.
    J Neurosci. 1994 Mar;14(3 Pt 1):1251-61 PMID: 8120623
  21. Adenylyl cyclases and the interaction between calcium and cAMP signalling.
    Nature. 1995 Mar 30;374(6521):421-4 PMID: 7700350
  22. Serotonin inhibits induction of long-term potentiation at commissural synapses in hippocampus.
    Brain Res. 1993 Mar 26;606(2):304-8 PMID: 8387861
  23. Autoradiographic localization of dopamine uptake sites in the rat brain with 3H-GBR 12935.
    J Neural Transm Gen Sect. 1992;87(1):1-14 PMID: 1346964
  24. A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory.
    Proc Natl Acad Sci U S A. 1989 Dec;86(23):9574-8 PMID: 2556718
  25. A framework for mesencephalic dopamine systems based on predictive Hebbian learning.
    J Neurosci. 1996 Mar 1;16(5):1936-47 PMID: 8774460
  26. Visualization of dopamine D1, D2 and D3 receptor mRNAs in human and rat brain.
    Neurochem Int. 1992 Mar;20 Suppl:33S-43S PMID: 1365451
  27. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons.
    Science. 1993 Jun 11;260(5114):1661-4 PMID: 8389057
  28. Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices.
    Brain Res. 1990 Jul 2;522(1):69-75 PMID: 1977494
  29. Coactivation of D1 and D2 dopamine receptors is required for long-term synaptic depression in the striatum.
    Neurosci Lett. 1992 Aug 3;142(1):95-9 PMID: 1357611
  30. Induction of long-lasting potentiation by sequenced applications of isoproterenol.
    Neuroreport. 1994 Jan 31;5(5):657-60 PMID: 7912965
  31. Low-frequency stimulation at the troughs of theta-oscillation induces long-term depression of previously potentiated CA1 synapses.
    J Neurophysiol. 1996 Feb;75(2):877-84 PMID: 8714660
  32. Beta-adrenergic regulation of synaptic NMDA receptors by cAMP-dependent protein kinase.
    Neuron. 1996 Feb;16(2):415-21 PMID: 8789956
  33. Hippocampal long-term potentiation is induced by pairing single afferent volleys with intracellularly injected depolarizing current pulses.
    Acta Physiol Scand. 1986 Feb;126(2):317-9 PMID: 3705989
  34. Factors regulating the magnitude of long-term potentiation induced by theta pattern stimulation.
    Brain Res. 1992 Dec 11;598(1-2):173-84 PMID: 1486479
  35. Differential coupling of D1 and D5 dopamine receptors to guanine nucleotide binding proteins in transfected GH4C1 rat somatomammotrophic cells.
    J Neurochem. 1995 May;64(5):2118-24 PMID: 7722495
  36. Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons.
    Nature. 1994 Apr 28;368(6474):853-6 PMID: 8159245
  37. Contrasting properties of two forms of long-term potentiation in the hippocampus.
    Nature. 1995 Sep 14;377(6545):115-8 PMID: 7675078
  38. Forskolin: its biological and chemical properties.
    Adv Cyclic Nucleotide Protein Phosphorylation Res. 1986;20:1-150 PMID: 3028083
  39. Acetylcholine release in the hippocampus: regulation by monoaminergic afferents as assessed by in vivo microdialysis.
    Brain Res. 1992 Jul 3;584(1-2):132-40 PMID: 1355389
  40. Dopamine modulates the slow Ca(2+)-activated K+ current IAHP via cyclic AMP-dependent protein kinase in hippocampal neurons.
    J Neurophysiol. 1995 Dec;74(6):2749-53 PMID: 8747230
  41. N-methyl-d-aspartate receptors modulate extracellular dopamine concentration and metabolism in rat hippocampus and striatum in vivo.
    Brain Res. 1994 Jan 28;635(1-2):312-6 PMID: 8173968
  42. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression.
    Nature. 1994 Jun 9;369(6480):486-8 PMID: 7515479
  43. nMDA receptor activation increases cyclic AMP in area CA1 of the hippocampus via calcium/calmodulin stimulation of adenylyl cyclase.
    J Neurochem. 1993 Nov;61(5):1933-42 PMID: 7901336
  44. Structure and function of cyclic nucleotide-dependent protein kinases.
    Annu Rev Physiol. 1994;56:237-72 PMID: 8010741
  45. Two-stage model of memory trace formation: a role for "noisy" brain states.
    Neuroscience. 1989;31(3):551-70 PMID: 2687720
  46. Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein.
    Science. 1996 Mar 15;271(5255):1589-92 PMID: 8599116
  47. Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task.
    J Neurosci. 1993 Mar;13(3):900-13 PMID: 8441015
  48. The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro.
    Neurosci Lett. 1991 Aug 5;129(1):111-4 PMID: 1833673
  49. D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus.
    Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2446-50 PMID: 7708662
  50. A novel cholinergic induction of long-term potentiation in rat hippocampus.
    J Neurophysiol. 1994 Oct;72(4):2034-40 PMID: 7823117
  51. Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration.
    J Neurosci. 1996 Mar 1;16(5):1922-35 PMID: 8774459
  52. Muscarinic depression of synaptic transmission and blockade of norepinephrine-induced long-lasting potentiation in the dentate gyrus.
    Neuroscience. 1993 May;54(2):377-89 PMID: 7687752
  53. Toward a modern theory of adaptive networks: expectation and prediction.
    Psychol Rev. 1981 Mar;88(2):135-70 PMID: 7291377
  54. The maintenance of hippocampal long-term potentiation is paralleled by a dopamine-dependent increase in glycoprotein fucosylation.
    Neurochem Int. 1992 Oct;21(3):403-8 PMID: 1338901
  55. Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro.
    Neuron. 1995 Nov;15(5):1053-63 PMID: 7576649
  56. Dopamine D2 receptor expression in hippocampus and parahippocampal cortex of rat, cat, and human in relation to tyrosine hydroxylase-immunoreactive fibers.
    Hippocampus. 1994 Jun;4(3):354-73 PMID: 7842057
  57. Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region.
    Neuron. 1995 Dec;15(6):1403-14 PMID: 8845163
  58. Distribution of D5 dopamine receptor mRNA in rat brain.
    Neurosci Lett. 1992 Oct 12;145(2):209-12 PMID: 1465219
  59. Dopamine modulates CA1 hippocampal neurons by elevating the threshold for spike generation: an in vitro study.
    Neuroscience. 1984 Dec;13(4):1105-16 PMID: 6527792
  60. Voltage-sensitive adenylyl cyclase activity in cultured neurons. A calcium-independent phenomenon.
    J Biol Chem. 1995 Jun 16;270(24):14340-6 PMID: 7782293
  61. Value-dependent selection in the brain: simulation in a synthetic neural model.
    Neuroscience. 1994 Mar;59(2):229-43 PMID: 8008189
  62. Modulatory actions of dopamine on NMDA receptor-mediated responses are reduced in D1A-deficient mutant mice.
    J Neurosci. 1996 Sep 15;16(18):5870-82 PMID: 8795639
  63. Re-examination of the ontogeny in the gene expression of DARPP-32 in the rat brain.
    Brain Res Mol Brain Res. 1994 Aug;25(1-2):67-72 PMID: 7984053
  64. Two components of long-term potentiation induced by different patterns of afferent activation.
    Nature. 1990 Oct 4;347(6292):477-9 PMID: 1977084
  65. D1 dopamine receptor immunoreactivity in human and monkey cerebral cortex: predominant and extrasynaptic localization in dendritic spines.
    Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5720-4 PMID: 7911245
  66. Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat.
    Brain Res Bull. 1994;33(4):445-52 PMID: 8124582
  67. Localization of dopamine D2 receptor mRNA with non-radioactive in situ hybridization histochemistry.
    Neurosci Lett. 1992 Aug 17;142(2):223-7 PMID: 1454220
  68. Forskolin: a specific stimulator of adenylyl cyclase or a diterpene with multiple sites of action?
    Trends Pharmacol Sci. 1989 Nov;10(11):442-7 PMID: 2692256
  69. Location and molecular cloning of D1 dopamine receptor.
    Neurochem Int. 1992 Mar;20 Suppl:9S-15S PMID: 1365464
  70. Novel dopamine receptors half a decade later.
    Trends Pharmacol Sci. 1995 Aug;16(8):270-5 PMID: 7482988
  71. Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials.
    J Neurosci. 1987 Mar;7(3):774-80 PMID: 2881989
  72. Dopamine action on hippocampal pyramidal cells.
    J Neurosci. 1982 Apr;2(4):415-23 PMID: 6279796
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1996-12-01
Pages
7478-86
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6579102
Subset
IM
Grants
NINDS NIH HHS · R01 NS027337 · United States
NINDS NIH HHS · 5 R01 NS27337-7 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]