Bidirectional regulation of synaptic plasticity in the basolateral amygdala induced by the D1-like family of dopamine receptors and group II metabotropic glutamate receptors

Journal of Physiology

Volumn 592, Issue 19, 2014, Pages 4329-4351

  Li, Chenchen ^a,b   Rainnie, Donald G ^a,b  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 2 CYANO 3 (3,4 DIHYDROPHENYL) N (PHENYLMETHYL) 2 PROPENAMIDE; 2,2,2 TRIFLUORO N [4 (2 METHOXYPHENOXY)PHENYL] N (3 PYRIDINYLMETHYL)ETHANESULFONAMIDE HYDROCHLORIDE; 2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; 3 (2 CARBOXYPIPERAZIN 4 YL) PROPYL 1 PHOSPHONIC ACID; 4 AMINO 2 OXABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID; 8 BROMO CYCLIC AMP; 8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; ADENYLATE CYCLASE; AMIDE; CLOZAPINE N OXIDE; DOPAMINE; DOPAMINE 1 RECEPTOR; FORSKOLIN; GLUTAMATE RECEPTOR 2; N (2 PHENYLCYCLOPENTYL) AZACYCLOTRIDEC 1 EN 2 AMINE HYDROCHLORIDE; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; NEOMYCIN; PHOSPHONIC ACID DERIVATIVE; SULFONAMIDE; U 73211; UNCLASSIFIED DRUG; AMINO ACID RECEPTOR BLOCKING AGENT; AMINO ACID RECEPTOR STIMULATING AGENT; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; BRAIN NERVE CELL; CELL TYPE; CONTROLLED STUDY; ENZYME ACTIVITY; FEAR; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; RAT; RECEPTOR BLOCKING; REGULATORY MECHANISM; REINFORCEMENT; SIGNAL TRANSDUCTION; AMYGDALOID NUCLEUS; ANIMAL; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; METABOLISM; NERVE CELL; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPSE;

AMYGDALA; ANIMALS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; NEURONAL PLASTICITY; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D1; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES;

EID: 84908565905     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.277715     Document Type: Article

References (87)

1. Abraham WC & Bear MF (1996). Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19, 126-130.
2. Andersen PH, Gingrich JA, Bates MD, Dearry A, Falardeau P, Senogles SE & Caron MG (1990). Dopamine receptor subtypes: beyond the D1/D2 classification. Trends Pharmacol Sci 11, 231-236.
3. Armbruster BN, Li X, Pausch MH, Herlitze S & Roth BL (2007). Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc Natl Acad Sci U S A 104, 5163-5168.
4. Bear MF & Malenka RC (1994). Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4, 389-399.
5. Bienenstock EL, Cooper LN & Munro PW (1982). Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2, 32-48.
6. Blaise JH & Bronzino JD (2003). Effects of stimulus frequency and age on bidirectional synaptic plasticity in the dentate gyrus of freely moving rats. Exp Neurol 182, 497-506.
7. Braga MF, Aroniadou-Anderjaska V & Li H (2004). The physiological role of kainate receptors in the amygdala. Mol Neurobiol 30, 127-141.
8. Carlsson A & Lindqvist M (1963). Effect of chlorpromazine or haloperidol on formation of 3methoxytyramine and normetanephrine in mouse brain. Acta Pharmacol Toxicol (Copenh) 20, 140-144.
9. Chen CY, Ling Eh EH, Horowitz JM & Bonham AC (2002). Synaptic transmission in nucleus tractus solitarius is depressed by Group II and III but not Group I presynaptic metabotropic glutamate receptors in rats. J Physiol 538, 773-786.
10. Clark D & White FJ (1987). D1 dopamine receptor - the search for a function: a critical evaluation of the D1/D2 dopamine receptor classification and its functional implications. Synapse 1, 347-388.
11. Conn PJ & Pin JP (1997). Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37, 205-237.
12. Dalton GL, Wu DC, Wang YT, Floresco SB & Phillips AG (2012). NMDA GluN2A and GluN2B receptors play separate roles in the induction of LTP and LTD in the amygdala and in the acquisition and extinction of conditioned fear. Neuropharmacology 62, 797-806.
13. Domenici MR, Berretta N & Cherubini E (1998). Two distinct forms of long-term depression coexist at the mossy fiber-CA3 synapse in the hippocampus during development. Proc Natl Acad Sci U S A 95, 8310-8315.
14. Ehrlich DE, Ryan SJ, Hazra R, Guo JD & Rainnie DG (2013). Postnatal maturation of GABAergic transmission in the rat basolateral amygdala. J Neurophysiol 110, 926-941.
15. Ehrlich DE, Ryan SJ & Rainnie DG (2012). Postnatal development of electrophysiological properties of principal neurons in the rat basolateral amygdala. J Physiol 590, 4819-4838.
16. Etkin A & Wager TD (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry 164, 1476-1488.
17. Faber DS & Korn H (1991). Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys. J. 60, 1288-1294.
18. Fadok JP, Dickerson TM & Palmiter RD (2009). Dopamine is necessary for cue-dependent fear conditioning. J Neurosci 29, 11089-11097.
19. Fourcaudot E, Gambino F, Humeau Y, Casassus G, Shaban H, Poulain B & Lüthi A (2008). cAMP/PKA signaling and RIM1α mediate presynaptic LTP in the lateral amygdala. Proc Natl Acad Sci U S A 105, 15130-15135.
20. Froc DJ & Racine RJ (2005). Interactions between LTP- and LTD-inducing stimulation in the sensorimotor cortex of the awake freely moving rat. J Neurophysiol 93, 548-556.
21. Genoux D, Bezerra P & Montgomery JM (2011). Intra-spaced stimulation and protein phosphatase 1 dictate the direction of synaptic plasticity. Eur J Neurosci 33, 1761-1770.
22. Gerber G, Zhong J, Youn D & Randic M (2000). Group II and group III metabotropic glutamate receptor agonists depress synaptic transmission in the rat spinal cord dorsal horn. Neuroscience 100, 393-406.
23. Gisabella B, Rowan MJ & Anwyl R (2003). Mechanisms underlying the inhibition of long-term potentiation by preconditioning stimulation in the hippocampus in vitro. Neuroscience 121, 297-305.
24. Goosens KA & Maren S (2002). Long-term potentiation as a substrate for memory: evidence from studies of amygdaloid plasticity and Pavlovian fear conditioning. Hippocampus 12, 592-599.
25. 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, 262-272.
26. Grillon C, Cordova J, Levine LR & Morgan CA, 3rd (2003). Anxiolytic effects of a novel group II metabotropic glutamate receptor agonist (LY354740) in the fear-potentiated startle paradigm in humans. Psychopharmacology (Berl) 168, 446-454.
27. Hancock PJS, Leslie S., Phillips & William A (1991). A biologically supported error-correcting learning rule. Neural Computation 3, 201-212.
28. Helton DR, Tizzano JP, Monn JA, Schoepp DD & Kallman MJ (1998). Anxiolytic and side-effect profile of LY354740: a potent, highly selective, orally active agonist for group II metabotropic glutamate receptors. J Pharmacol Exp Ther 284, 651-660.
29. Hengen KB, Lambo ME, Van Hooser SD, Katz DB & Turrigiano GG (2013). Firing rate homeostasis in visual cortex of freely behaving rodents. Neuron 80, 335-342.
30. Huang YY & Kandel ER (1998). Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21, 169-178.
31. Inglis FM & Moghaddam B (1999). Dopaminergic innervation of the amygdala is highly responsive to stress. J Neurochem 72, 1088-1094.
32. Ji G & Neugebauer V (2012). Modulation of medial prefrontal cortical activity using in vivo recordings and optogenetics. Mol Brain 5, 36.
33. Jouvenceau A, Hedou G, Potier B, Kollen M, Dutar P & Mansuy IM (2006). Partial inhibition of PP1 alters bidirectional synaptic plasticity in the hippocampus. Eur J Neurosci 24, 564-572.
34. Jovanovic T & Ressler KJ. How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. Am J Psychiatry 167, 648-662.
35. Kamiya H, Shinozaki H & Yamamoto C (1996). Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. J Physiol 493, 447-455.
36. Kamiya H & Yamamoto C (1997). Phorbol ester and forskolin suppress the presynaptic inhibitory action of group-II metabotropic glutamate receptor at rat hippocampal mossy fibre synapse. Neuroscience 80, 89-94.
37. Kasanetz F, Deroche-Gamonet V, Berson N, Balado E, Lafourcade M, Manzoni O & Piazza PV (2010). Transition to addiction is associated with a persistent impairment in synaptic plasticity. Science 328, 1709-1712.
38. Kemp N, McQueen J, Faulkes S & Bashir ZI (2000). Different forms of LTD in the CA1 region of the hippocampus: role of age and stimulus protocol. Eur J Neurosci 12, 360-366.
39. Kienast T, Hariri AR, Schlagenhauf F, Wrase J, Sterzer P, Buchholz HG, Smolka MN, Gründer G, Cumming P, Kumakura Y, Bartenstein P, Dolan RJ & Heinz A (2008). Dopamine in amygdala gates limbic processing of aversive stimuli in humans. Nat Neurosci 11, 1381-1382.
40. Kim MH, Choi J, Yang J, Chung W, Kim JH, Paik SK, Kim K, Han S, Won H, Bae YS, Cho SH, Seo J, Bae YC, Choi SY & Kim E (2009). Enhanced NMDA receptor-mediated synaptic transmission, enhanced long-term potentiation, and impaired learning and memory in mice lacking IRSp53. J Neurosci 29, 1586-1595.
41. Krystal JH, Mathew SJ, D'Souza DC, Garakani A, Gunduz-Bruce H & Charney DS (2010). Potential psychiatric applications of metabotropic glutamate receptor agonists and antagonists. CNS Drugs 24, 669-693.
42. 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, 128-136.
43. Li C, Dabrowska J, Hazra R & Rainnie DG (2011). Synergistic activation of dopamine D1 and TrkB receptors mediate gain control of synaptic plasticity in the basolateral amygdala. PLoS One 6, e26065.
44. Li H, Weiss SR, Chuang DM, Post RM & Rogawski MA (1998). Bidirectional synaptic plasticity in the rat basolateral amygdala: characterization of an activity-dependent switch sensitive to the presynaptic metabotropic glutamate receptor antagonist 2S-α-ethylglutamic acid. J Neurosci 18, 1662-1670.
45. Likhtik E, Pelletier JG, Paz R & Pare D (2005). Prefrontal control of the amygdala. J Neurosci 25, 7429-7437.
46. Lin CH, Lee CC, Huang YC, Wang SJ & Gean PW (2005). Activation of group II metabotropic glutamate receptors induces depotentiation in amygdala slices and reduces fear-potentiated startle in rats. Learn Mem 12, 130-137.
47. Lin HC, Wang SJ, Luo MZ & Gean PW (2000). Activation of group II metabotropic glutamate receptors induces long-term depression of synaptic transmission in the rat amygdala. J Neurosci 20, 9017-9024.
48. Lovinger DM & McCool BA (1995). Metabotropic glutamate receptor-mediated presynaptic depression at corticostriatal synapses involves mGLuR2 or 3. J Neurophysiol 73, 1076-1083.
49. Maccaferri G, Toth K & McBain CJ (1998). Target-specific expression of presynaptic mossy fibre plasticity. Science 279, 1368-1370.
50. Mahon S & Charpier S (2012). Bidirectional plasticity of intrinsic excitability controls sensory inputs efficiency in layer 5 barrel cortex neurons in vivo. J Neurosci 32, 11377-11389.
51. Malenka RC (1994). Synaptic plasticity in the hippocampus: LTP and LTD. Cell 78, 535-538.
52. Malleret G, Alarcon JM, Martel G, Takizawa S, Vronskaya S, et al. (2010). Bidirectional regulation of hippocampal long-term synaptic plasticity and its influence on opposing forms of memory. J Neurosci 30, 3813-3825.
53. Maroun M (2006). Stress reverses plasticity in the pathway projecting from the ventromedial prefrontal cortex to the basolateral amygdala. Eur J Neurosci 24, 2917-2922.
54. Martin M, Chen BT, Hopf FW, Bowers MS & Bonci A (2006). Cocaine self-administration selectively abolishes LTD in the core of the nucleus accumbens. Nat Neurosci 9, 868-869.
55. Matsuda Y, Marzo A & Otani S (2006). The presence of background dopamine signal converts long-term synaptic depression to potentiation in rat prefrontal cortex. J Neurosci 26, 4803-4810.
56. Mayford M, Wang J, Kandel ER & O'Dell TJ (1995). CaMKII regulates the frequency-response function of hippocampal synapses for the production of both LTD and LTP. Cell 81, 891-904.
57. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RG, Morrison JH, O'Dell TJ & Grant SG (1998). Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396, 433-439.
58. Muly EC, Mania I, Guo JD & Rainnie DG (2007). Group II metabotropic glutamate receptors in anxiety circuitry: correspondence of physiological response and subcellular distribution. J Comp Neurol 505, 682-700.
59. Muly EC, Senyuz M, Khan ZU, Guo JD, Hazra R & Rainnie DG (2009). Distribution of D1 and D5 dopamine receptors in the primate and rat basolateral amygdala. Brain Struct Funct 213, 375-393.
60. Nicolas CS, Peineau S, Amici M, Csaba Z, Fafouri A, Javalet C, Collett VJ, Hildebrandt L, Seaton G, Choi SL, Sim SE, Bradley C, Lee K, Zhuo M, Kaang BK, Gressens P, Dournaud P, Fitzjohn SM, Bortolotto ZA, Cho K & Collingridge GL (2012). The Jak/STAT pathway is involved in synaptic plasticity. Neuron 73, 374-390.
61. Pare D & Collins DR (2000). Neuronal correlates of fear in the lateral amygdala: multiple extracellular recordings in conscious cats. J Neurosci 20, 2701-2710.
62. Patil ST, Zhang L, Martenyi F, Lowe SL, Jackson KA, Andreev BV, Avedisova AS, Bardenstein LM, Gurovich IY, Morozova MA, Mosolov SN, Neznanov NG, Reznik AM, Smulevich AB, Tochilov VA, Johnson BG, Monn JA & Schoepp DD (2007). Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized Phase 2 clinical trial. Nat Med 13, 1102-1107.
63. Prezeau L, Manzoni O, Homburger V, Sladeczek F, Curry K & Bockaert J (1992). Characterization of a metabotropic glutamate receptor: direct negative coupling to adenylyl cyclase and involvement of a pertussis toxin-sensitive G protein. Proc Natl Acad Sci U S A 89, 8040-8044.
64. Rainnie DG, Asprodini EK & Shinnick-Gallagher P (1993). Intracellular recordings from morphologically identified neurons of the basolateral amygdala. J Neurophysiol 69, 1350-1362.
65. Rainnie DG, Holmes KH & Shinnick-Gallagher P (1994). Activation of postsynaptic metabotropic glutamate receptors by trans-ACPD hyperpolarizes neurons of the basolateral amygdala. J Neurosci 14, 7208-7220.
66. Rainnie DG & Shinnick-Gallagher P (1992). Trans-ACPD and L-APB presynaptically inhibit excitatory glutamatergic transmission in the basolateral amygdala (BLA). Neurosci Lett 139, 87-91.
67. Rauch AV, Reker M, Ohrmann P, Pedersen A, Bauer J, Dannlowski U, Harding L, Koelkebeck K, Konrad C, Kugel H, Arolt V, Heindel W & Suslow T (2010). Increased amygdala activation during automatic processing of facial emotion in schizophrenia. Psychiatry Res 182, 200-206.
68. 2+ channels in metabotropic glutamate receptor 2/3-dependent presynaptic long-term depression at nucleus accumbens synapses. J Neurosci 22, 4346-4356.
69. Rogan MT, Staubli UV & LeDoux JE (1997). Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390, 604-607.
70. Rosenkranz JA & Grace AA (1999). Modulation of basolateral amygdala neuronal firing and afferent drive by dopamine receptor activation in vivo. J Neurosci 19, 11027-11039.
71. Rumberger A, Schmidt M, Lohmann H & Hoffmann KP (1998). Correlation of electrophysiology, morphology, and functions in corticotectal and corticopretectal projection neurons in rat visual cortex. Exp Brain Res 119, 375-390.
72. Schaffhauser H, Cai Z, Hubalek F, Macek TA, Pohl J, Murphy TJ & Conn PJ (2000). cAMP-dependent protein kinase inhibits mGluR2 coupling to G-proteins by direct receptor phosphorylation. J Neurosci 20, 5663-5670.
73. Schneider F, Weiss U, Kessler C, Salloum JB, Posse S, Grodd W & Müller-Gärtner HW (1998). Differential amygdala activation in schizophrenia during sadness. Schizophr Res 34, 133-142.
74. Sejnowski TJ (1977). Statistical constraints on synaptic plasticity. J Theor Biol 69, 385-389.
75. Senn V, Wolff SB, Herry C, Grenier F, Ehrlich I, Gründemann J, Fadok JP, Müller C, Letzkus JJ & Lüthi A (2014). Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron 81, 428-437.
76. Shekhar A & Keim SR (2000). LY354740, a potent group II metabotropic glutamate receptor agonist prevents lactate-induced panic-like response in panic-prone rats. Neuropharmacology 39, 1139-1146.
77. Stein MB, Simmons AN, Feinstein JS & Paulus MP (2007). Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. Am J Psychiatry 164, 318-327.
78. Takahashi H, Takano H, Kodaka F, Arakawa R, Yamada M, Otsuka T, Hirano Y, Kikyo H, Okubo Y, Kato M, Obata T, Ito H & Suhara T (2010). Contribution of dopamine D1 and D2 receptors to amygdala activity in human. J Neurosci 30: 3043-3047.
79. Tsubo Y, Isomura Y & Fukai T (2013). Neural dynamics and information representation in microcircuits of motor cortex. Front Neural Circuits 7, 85.
80. Volkow ND, Fowler JS, Wang GJ & Swanson JM (2004). Dopamine in drug abuse and addiction: results from imaging studies and treatment implications. Mol Psychiatry 9, 557-569.
81. Walker DL & Davis M (2002). The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction. Pharmacol Biochem Behav 71, 379-392.
82. Walker DL, Rattiner LM & Davis M (2002). Group II metabotropic glutamate receptors within the amygdala regulate fear as assessed with potentiated startle in rats. Behav Neurosci 116, 1075-1083.
83. Wang HY, Undie AS & Friedman E (1995). Evidence for the coupling of Gq protein to D1-like dopamine sites in rat striatum: possible role in dopamine-mediated inositol phosphate formation. Mol Pharmacol 48, 988-994.
84. Wang SJ & Gean PW (1999). Long-term depression of excitatory synaptic transmission in the rat amygdala. J Neurosci 19, 10656-10663.
85. Willshaw D & Dayan P (1990). Optimal plasticity from matrix memories: what goes up must come down. Neural Comput 2, 85-93.
86. Yang TT, Simmons AN, Matthews SC, Tapert SF, Frank GK, Max JE, Bischoff-Grethe A, Lansing AE, Brown G, Strigo IA, Wu J & Paulus MP (2010). Adolescents with major depression demonstrate increased amygdala activation. J Am Acad Child Adolesc Psychiatry 49, 42-51.
87. Zhong M, Wang X, Xiao J, Yi J, Zhu X, Liao J, Wang W & Yao S (2011). Amygdala hyperactivation and prefrontal hypoactivation in subjects with cognitive vulnerability to depression. Biol Psychol 88, 233-242.