Dopamine Receptors and Groups I and II mGluRs Cooperate for Long-Term Depression Induction in Rat Prefrontal Cortex through Converging Postsynaptic Activation of MAP Kinases

Tetanic stimuli to layer I–II afferents in rat prefrontal cortex induced long-term depression (LTD) of layer I–II to layer V pyramidal neuron glutamatergic synapses when tetani were coupled to bath application of dopamine. This LTD was blocked by the following metabotropic glutamate receptor (mGluR) antagonists coapplied with dopamine: (S)-α-methyl-4-carboxyphenylglycine (MCPG; group I and II antagonist), (RS)-1-aminoindan-1,5-dicarboxylic acid (AIDA; group I antagonist), or (RS)-α-methylserine-O-phosphate monophenyl ester (MSOPPE; group II antagonist). This suggests that the dopamine-facilitated LTD requires synaptic activation of groups I and II mGluRs during tetanus. LTD could also be induced by coupling tetani to bath application of groups I and II mGluR agonist (1S,3R)-1-aminocyclopentane-1,3-dicarboxylic acid (1S,3R-ACPD). In the next series of experiments, coapplication of dopamine and 1S,3R-ACPD, but not application of either drug alone, consistently induced LTD without tetani or even single test stimuli during drug application, suggesting that coactivation of dopamine receptors and the mGluRs is sufficient for LTD induction. Immunoblot analyses with anti-active mitogen-activated protein kinases (MAP-Ks) revealed that D1 receptors, D2 receptors, group I mGluRs, and group II mGluRs all contribute to MAP-K activation in prefrontal cortex, and that combined activation of dopamine receptors and mGluRs synergistically or additively activate MAP-Ks. Consistently, LTD by dopamine + 1S,3R-ACPD coapplication, as well as the two other forms of LTD (LTD by dopamine + tetani and LTD by 1S,3R-ACPD + tetani), was blocked by bath application of MAP-K kinase inhibitor PD98059. LTD by dopamine + 1S,3R-ACPD coapplication was also blocked by postsynaptic injection of synthetic MAP-K substrate peptide. Our results suggest that dopamine receptors and groups I and II mGluRs cooperate to induce LTD through converging postsynaptic activation of MAP-Ks.

[1]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[2]  H. Towbin,et al.  Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[3]  H. Simon,et al.  Dopaminergic A10 neurones are involved in cognitive functions , 1980, Nature.

[4]  J. Glowinski,et al.  The mesocortico-prefrontal dopaminergic neurons , 1984, Trends in Neurosciences.

[5]  Bryan Kolb,et al.  Functions of the frontal cortex of the rat: A comparative review , 1984, Brain Research Reviews.

[6]  F. Crépel,et al.  Use‐dependent changes in synaptic efficacy in rat prefrontal neurons in vitro. , 1990, The Journal of physiology.

[7]  M. Martres,et al.  Dopamine activation of the arachidonic acid cascade as a basis for D1D2 receptor synergism , 1991, Nature.

[8]  S. Nakanishi,et al.  A family of metabotropic glutamate receptors , 1992, Neuron.

[9]  S. Nakanishi,et al.  Molecular characterization of a novel metabotropic glutamate receptor mGluR5 coupled to inositol phosphate/Ca2+ signal transduction. , 1992, The Journal of biological chemistry.

[10]  Y. Ben-Ari,et al.  Quisqualate Metabotropic Receptors Modulate NMDA Currents and Facilitate Induction of Long‐Term Potentiation Through Protein Kinase C , 1992, The European journal of neuroscience.

[11]  Y. Ben-Ari,et al.  Biochemical correlates of long-term potentiation in hippocampal synapses. , 1993, International review of neurobiology.

[12]  H. Shinozaki,et al.  A novel metabotropic glutamate receptor agonist: marked depression of monosynaptic excitation in the newborn rat isolated spinal cord , 1993, British journal of pharmacology.

[13]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[14]  T. Dawson,et al.  Differential localization of phosphoinositide-linked metabotropic glutamate receptor (mGluR1) and the inositol 1,4,5-trisphosphate receptor in rat brain , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  N. Kato.  Dependence of long-term depression on postsynaptic metabotropic glutamate receptors in visual cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[16]  M. Masu,et al.  Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4 , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  G. Collingridge,et al.  Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors , 1993, Nature.

[18]  P. Dent,et al.  Dual phosphorylation and autophosphorylation in mitogen-activated protein (MAP) kinase activation. , 1993, The Biochemical journal.

[19]  Y. Nishizuka,et al.  The protein kinase C family for neuronal signaling. , 1994, Annual review of neuroscience.

[20]  K. Reymann,et al.  Metabotropic glutamate receptor agonist DCG-IV as NMDA receptor agonist in immature rat hippocampal neurons. , 1994, European journal of pharmacology.

[21]  D. Law-Tho,et al.  Dopamine modulation of synaptic transmission in rat prefrontal cortex: an in vitro electrophysiological study , 1994, Neuroscience Research.

[22]  T. Nishikawa,et al.  Preferential Stimulation of Extracellular Release of Dopamine in Rat Frontal Cortex to Striatum Following Competitive Inhibition of the N‐Methyl‐d‐Aspartate Receptor , 1994, Journal of neurochemistry.

[23]  P. Goldman-Rakic,et al.  The role of D1-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task. , 1994, Journal of neurophysiology.

[24]  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.

[25]  D. Law-Tho,et al.  Dopamine favours the emergence of long-term depression versus long-term potentiation in slices of rat prefrontal cortex , 1995, Neuroscience Letters.

[26]  S. Iversen.  Interactions between excitatory amino acids and dopamine systems in the forebrain: implications for schizophrenia and Parkinson's disease. , 1995, Behavioural pharmacology.

[27]  E. Goldsmith,et al.  How MAP Kinases Are Regulated (*) , 1995, The Journal of Biological Chemistry.

[28]  P. Goldman-Rakic,et al.  Modulation of memory fields by dopamine Dl receptors in prefrontal cortex , 1995, Nature.

[29]  A. Bridges,et al.  A synthetic inhibitor of the mitogen-activated protein kinase cascade. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Philip R. Cohen,et al.  PD 098059 Is a Specific Inhibitor of the Activation of Mitogen-activated Protein Kinase Kinase in Vitro and in Vivo(*) , 1995, The Journal of Biological Chemistry.

[31]  J. Bockaert,et al.  Molecular, functional, and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: comparison with mGluR1 , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  P. Conn,et al.  Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1 , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  P. Goldman-Rakic.  Cellular basis of working memory , 1995, Neuron.

[34]  D. Piomelli,et al.  Dopamine D2 Receptors Potentiate Arachidonate Release via Activation of Cytosolic, Arachidonate‐Specific Phospholipase A2 , 1995, Journal of neurochemistry.

[35]  J. Bockaert,et al.  Phenylglycine derivatives discriminate between mGluR1- and mGluR5-mediated responses , 1995, Neuropharmacology.

[36]  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.

[37]  Etude in vitro des effets des catecholamines (dopamine et noradrenaline) sur la transmission et la plasticite synaptiques dans le cortex prefrontal du rat , 1995 .

[38]  A. N. van den Pol,et al.  Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain , 1995, The Journal of comparative neurology.

[39]  H. Tse,et al.  α-methyl derivatives of serine-O-phosphate as novel, selective competitive metabotropic glutamate receptor antagonists , 1996, Neuropharmacology.

[40]  H. Tse,et al.  Structure‐activity relationships of new agonists and antagonists of different metabotropic glutamate receptor subtypes , 1996, British journal of pharmacology.

[41]  Marc G Caron,et al.  Dopamine receptors and brain function , 1996, Neuropharmacology.

[42]  M. Roisin,et al.  Potassium Chloride Pulse Enhances Mitogen‐Activated Protein Kinase Activity in Rat Hippocampal Slices , 1996, Journal of neurochemistry.

[43]  M. Bear,et al.  Long-term depression in hippocampus. , 1996, Annual review of neuroscience.

[44]  J. David Sweatt,et al.  Activation of p42 Mitogen-activated Protein Kinase in Hippocampal Long Term Potentiation* , 1996, The Journal of Biological Chemistry.

[45]  R. Petralia,et al.  The metabotropic glutamate receptors, MGLUR2 and MGLUR3, show unique postsynaptic, presynaptic and glial localizations , 1996, Neuroscience.

[46]  P. Conn,et al.  Immunocytochemical localization of group III metabotropic glutamate receptors in the hippocampus with subtype-specific antibodies , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  K. Murakami,et al.  The Convergence of Axon Terminals from the Mediodorsal Thalamic Nucleus and Ventral Tegmental Area on Pyramidal Cells in Layer V of the Rat Prelimbic Cortex , 1996, The European journal of neuroscience.

[48]  F. Nicoletti,et al.  Metabotropic glutamate receptors: a new target for the therapy of neurodegenerative disorders? , 1996, Trends in Neurosciences.

[49]  L. Bindman,et al.  Metabotropic glutamate receptors are involved in long-term potentiation in isolated slices of rat medial frontal cortex. , 1997, Journal of neurophysiology.

[50]  M. Iyo,et al.  Decreased prefrontal dopamine D1 receptors in schizophrenia revealed by PET , 1997, Nature.

[51]  JaneR . Taylor,et al.  Supranormal Stimulation of D1 Dopamine Receptors in the Rodent Prefrontal Cortex Impairs Spatial Working Memory Performance , 1997, The Journal of Neuroscience.

[52]  R. Anwyl,et al.  mGluR II agonist inhibition of LTP induction, and mGluR II antagonist inhibition of LTD induction, in the dentate gyrus in vitro , 1997, Neuroreport.

[53]  P. Cohen,et al.  The search for physiological substrates of MAP and SAP kinases in mammalian cells. , 1997, Trends in cell biology.

[54]  G. Lombardi,et al.  Pharmacological characterization of 1-aminoindan-1,5-dicarboxylic acid, a potent mGluR1 antagonist. , 1997, The Journal of pharmacology and experimental therapeutics.

[55]  M. Cobb,et al.  Mitogen-activated protein kinase pathways. , 1997, Current opinion in cell biology.

[56]  H. Shinozaki,et al.  Ontogenetic and Pharmacological Studies on Metabotropic Glutamate Receptors Coupled to Phospholipase D Activation , 1997, Neuropharmacology.

[57]  JaneR . Taylor,et al.  Supranormal Stimulation of D 1 Dopamine Receptors in the Rodent Prefrontal Cortex Impairs Spatial Working Memory Performance , 1997 .

[58]  R. Nicoll,et al.  Two Distinct Forms of Long-Term Depression Coexist in CA1 Hippocampal Pyramidal Cells , 1997, Neuron.

[59]  Bita Moghaddam,et al.  Activation of Glutamatergic Neurotransmission by Ketamine: A Novel Step in the Pathway from NMDA Receptor Blockade to Dopaminergic and Cognitive Disruptions Associated with the Prefrontal Cortex , 1997, The Journal of Neuroscience.

[60]  J. Pin,et al.  Pharmacology and functions of metabotropic glutamate receptors. , 1997, Annual review of pharmacology and toxicology.

[61]  J. Desce,et al.  Dopamine facilitates long-term depression of glutamatergic transmission in rat prefrontal cortex , 1998, Neuroscience.

[62]  D. Manahan‐Vaughan,et al.  Subtype-specific involvement of metabotropic glutamate receptors in two forms of long-term potentiation in the dentate gyrus of freely moving rats , 1998, Neuroscience.

[63]  Group I metabotropic glutamate receptor (mGluR) agonists raise intracellular [Ca 2+ ] in medial frontal cortical neurones of the rat , 1998 .

[64]  J. Connor,et al.  Requirement of rapid Ca2+ entry and synaptic activation of metabotropic glutamate receptors for the induction of long‐term depression in adult rat hippocampus , 1998, The Journal of physiology.

[65]  E. Eriksson,et al.  Direct dopamine D2‐receptor‐mediated modulation of arachidonic acid release in transfected CHO cells without the concomitant administration of a Ca2+‐mobilizing agent , 1998, British journal of pharmacology.

[66]  B. Moghaddam,et al.  Corticolimbic Dopamine Neurotransmission Is Temporally Dissociated from the Cognitive and Locomotor Effects of Phencyclidine , 1998, The Journal of Neuroscience.

[67]  N. Daw,et al.  The Group III metabotropic glutamate receptor agonist, l-AP4, reduces EPSPs in some layers of rat visual cortex , 1998, Brain Research.

[68]  B. Moghaddam,et al.  Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. , 1998, Science.

[69]  A. Coogan,et al.  P42/44 MAP kinase inhibitor PD98059 attenuates multiple forms of synaptic plasticity in rat dentate gyrus in vitro. , 1999, Journal of neurophysiology.

[70]  J. Sweatt,et al.  The Mitogen-Activated Protein Kinase Cascade Couples PKA and PKC to cAMP Response Element Binding Protein Phosphorylation in Area CA1 of Hippocampus , 1999, The Journal of Neuroscience.

[71]  Takaaki AbeS,et al.  Molecular Characterization of a Novel Metabotropic Glutamate Receptor mGluR 5 Coupled to Inositol Phosphate / Ca 2 + Signal Transduction , 2001 .