D1/D5 Dopamine Receptor Activation Increases the Magnitude of Early Long-Term Potentiation at CA1 Hippocampal Synapses

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 ∼10, 15, and 20%, respectively). This D1/D5 effect was mimicked by a low dose (10 μm) of the adenylyl cyclase activator forskolin. The D1/D5 antagonist (+)SCH 23390 reduced early LTP. In catecholamine-depleted slices, LTP was smaller by ∼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.

[1]  P. Greengard,et al.  Advances in Cyclic Nucleotide and Protein Phosphorylation Research , 1975 .

[2]  J. Kebabian,et al.  Multiple receptors for dopamine , 1979, Nature.

[3]  A G Barto,et al.  Toward a modern theory of adaptive networks: expectation and prediction. , 1981, Psychological review.

[4]  D. Prince,et al.  Dopamine action on hippocampal pyramidal cells , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  V. Gribkoff,et al.  Modulation by dopamine of population responses and cell membrane properties of hippocampal CA1 neurons in vitro , 1984, Brain Research.

[6]  P. Calabresi,et al.  Dopamine modulates CA1 hippocampal neurons by elevating the threshold for spike generation: An in vitro study , 1984, Neuroscience.

[7]  J. Sarvey,et al.  Depletion of norepinephrine, but not serotonin, reduces long-term potentiation in the dentate gyrus of rat hippocampal slices , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  S. Pockett Dopamine changes the shape of action potentials in hippocampal pyramidal cells , 1985, Brain Research.

[9]  H. Wigström,et al.  Hippocampal long-term potentiation is induced by pairing single afferent volleys with intracellularly injected depolarizing current pulses. , 1986, Acta physiologica Scandinavica.

[10]  R. Nicoll,et al.  Dopamine decreases the calcium-activated afterhyperpolarization in hippocampal CA1 pyramidal cells , 1986, Brain Research.

[11]  J. Daly,et al.  Forskolin: its biological and chemical properties. , 1986, Advances in cyclic nucleotide and protein phosphorylation research.

[12]  Daly Jw,et al.  Forskolin: its biological and chemical properties. , 1986, Advances in cyclic nucleotide and protein phosphorylation research.

[13]  B. Gustafsson,et al.  Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  G. Buzsáki Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[15]  A. Laurenza,et al.  Forskolin: a specific stimulator of adenylyl cyclase or a diterpene with multiple sites of action? , 1989, Trends in pharmacological sciences.

[16]  J. Lisman,et al.  A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Lawrence M. Grover,et al.  Two components of long-term potentiation induced by different patterns of afferent activation , 1990, Nature.

[18]  U. Frey,et al.  Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices , 1990, Brain Research.

[19]  U. Frey,et al.  The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro , 1991, Neuroscience Letters.

[20]  Charles F. Stevens,et al.  Modulation of synaptic efficacy in field CA1 of the rat hippocampus by forskolin , 1992, Brain Research.

[21]  F. Angenstein,et al.  The maintenance of hippocampal long-term potentiation is paralleled by a dopamine-dependent increase in glycoprotein fucosylation , 1992, Neurochemistry International.

[22]  G. J. Horst,et al.  Localization of dopamine D2 receptor mRNA with non-radioactive in situ hybridization histochemistry , 1992, Neuroscience Letters.

[23]  D. Grandy,et al.  Distribution of D5 dopamine receptor mRNA in rat brain , 1992, Neuroscience Letters.

[24]  P. Calabresi,et al.  Coactivation of D1 and D2 dopamine receptors is required for long-term synaptic depression in the striatum , 1992, Neuroscience Letters.

[25]  G. Lynch,et al.  Factors regulating the magnitude of long-term potentiation induced by theta pattern stimulation , 1992, Brain Research.

[26]  A. Bjo¨rklund,et al.  Acetylcholine release in the hippocampus: regulation by monoaminergic afferents as assessed by in vivo microdialysis , 1992, Brain Research.

[27]  J. Gusella,et al.  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. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. Palacios,et al.  Visualization of dopamine D1, D2 and D3 receptor mRNA's in human and rat brain , 1992, Neurochemistry International.

[29]  M. Taylor,et al.  Long-term increases in excitability in the CA1 region of rat hippocampus induced by beta-adrenergic stimulation: possible mediation by cAMP , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  M. Caron,et al.  Location and molecular cloning of D1 dopamine receptor , 1992, Neurochemistry International.

[31]  D. Johnston,et al.  Serotonin inhibits induction of long-term potentiation at commissural synapses in hippocampus , 1993, Brain Research.

[32]  W. Schultz,et al.  Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  G. Gessa,et al.  Stimulation of both dopamine D1 and D2 receptors facilitates in vivo acetylcholine release in the hippocampus , 1993, Brain Research.

[34]  J. Sarvey,et al.  Muscarinic depression of synaptic transmission and blockade of norepinephrine-induced long-lasting potentiation in the dentate gyrus , 1993, Neuroscience.

[35]  P. O’Donnell,et al.  Dopaminergic modulation of dye coupling between neurons in the core and shell regions of the nucleus accumbens , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  E. Kandel,et al.  Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. , 1993, Science.

[37]  J. Sweatt,et al.  NMDA Receptor Activation Increases Cyclic AMP in Area CA1 of the Hippocampus via Calcium/Calmodulin Stimulation of Adenylyl Cyclase , 1993, Journal of neurochemistry.

[38]  J. Corbin,et al.  Structure and function of cyclic nucleotide-dependent protein kinases. , 1994, Annual review of physiology.

[39]  L. Fowler,et al.  N-methyl-d-aspartate receptors modulate extracellular dopamine concentration and metabolism in rat hippocampus and striatum in vivo , 1994, Brain Research.

[40]  D. Dahl,et al.  Induction of long-lasting potentiation by sequenced applications of isoproterenol. , 1994, Neuroreport.

[41]  M Segal,et al.  A novel cholinergic induction of long-term potentiation in rat hippocampus. , 1994, Journal of neurophysiology.

[42]  H. Sakagami,et al.  Re-examination of the ontogeny in the gene expression of DARPP-32 in the rat brain. , 1994, Brain research. Molecular brain research.

[43]  P S Goldman-Rakic,et al.  D1 dopamine receptor immunoreactivity in human and monkey cerebral cortex: predominant and extrasynaptic localization in dendritic spines. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Karl J. Friston,et al.  Value-dependent selection in the brain: Simulation in a synthetic neural model , 1994, Neuroscience.

[45]  J. Joyce,et al.  Dopamine D2 receptor expression in hippocampus and parahippocampal cortex of rat, cat, and human in relation to tyrosine hydroxylase‐immunoreactive fibers , 1994, Hippocampus.

[46]  C. Yokoyama,et al.  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 , 1994, The Journal of comparative neurology.

[47]  JW Polli,et al.  Expression of a calmodulin-dependent phosphodiesterase isoform (PDE1B1) correlates with brain regions having extensive dopaminergic innervation , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  S. Kaneko,et al.  Inhibitory influence via 5-HT3 receptors on the induction of LTP in mossy fiber-CA3 system of guinea-pig hippocampal slices , 1994, Neuroscience Research.

[49]  J. Lisman The CaM kinase II hypothesis for the storage of synaptic memory , 1994, Trends in Neurosciences.

[50]  Mark G. Packard,et al.  Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat , 1994, Brain Research Bulletin.

[51]  Christian Rosenmund,et al.  Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons , 1994, Nature.

[52]  B. O'dowd,et al.  Heterogeneous tissue-specific transcription of dopamine receptor subtype messenger RNA in rat brain. , 1994, Brain research. Molecular brain research.

[53]  R. Malenka,et al.  Involvement of a calcineurin/ inhibitor-1 phosphatase cascade in hippocampal long-term depression , 1994, Nature.

[54]  N. Mons,et al.  Selective expression of one Ca(2+)-inhibitable adenylyl cyclase in dopaminergically innervated rat brain regions. , 1994, Brain research. Molecular brain research.

[55]  E. Kandel,et al.  D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[56]  D. Grandy,et al.  Differential Coupling of D1 and D5 Dopamine Receptors to Guanine Nucleotide Binding Proteins in Transfected GH4C1 Rat Somatomammotrophic Cells , 1995, Journal of neurochemistry.

[57]  R. Nicoll,et al.  Contrasting properties of two forms of long-term potentiation in the hippocampus , 1995, Nature.

[58]  N. Mons,et al.  Adenylyl cyclases and the interaction between calcium and cAMP signalling , 1995, Nature.

[59]  J. Lisman,et al.  Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro , 1995, Neuron.

[60]  J F Storm,et al.  Dopamine modulates the slow Ca(2+)-activated K+ current IAHP via cyclic AMP-dependent protein kinase in hippocampal neurons. , 1995, Journal of neurophysiology.

[61]  H. Miyakawa,et al.  Activation of dopamine D1 receptors enhances long-term depression of synaptic transmission induced by low frequency stimulation in rat hippocampal CA1 neurons , 1995, Neuroscience Letters.

[62]  R. Iyengar,et al.  Postsynaptic CAMP pathway gates early LTP in hippocampal CA1 region , 1995, Neuron.

[63]  P. Sokoloff,et al.  Novel dopamine receptors half a decade later. , 1995, Trends in pharmacological sciences.

[64]  L. Langeberg,et al.  Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. , 1995, Science.

[65]  E. Villacres,et al.  Voltage-sensitive Adenylyl Cyclase Activity in Cultured Neurons. A CALCIUM-INDEPENDENT PHENOMENON (*) , 1995, The Journal of Biological Chemistry.

[66]  P. Goldman-Rakic,et al.  Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  CR Yang,et al.  Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[69]  R. Wise,et al.  Addictive drugs and brain stimulation reward. , 1996, Annual review of neuroscience.

[70]  L. Langeberg,et al.  Coordination of Three Signaling Enzymes by AKAP79, a Mammalian Scaffold Protein , 1996, Science.

[71]  J. Lisman,et al.  Low-frequency stimulation at the troughs of theta-oscillation induces long-term depression of previously potentiated CA1 synapses. , 1996, Journal of neurophysiology.

[72]  H. C. Cromwell,et al.  Modulatory Actions of Dopamine on NMDA Receptor-Mediated Responses Are Reduced in D1A-Deficient Mutant Mice , 1996, The Journal of Neuroscience.

[73]  C. Jahr,et al.  β-Adrenergic Regulation of Synaptic NMDA Receptors by cAMP-Dependent Protein Kinase , 1996, Neuron.