Reduced Threshold for Induction of LTP by Activation of Dopamine D1/D5 Receptors at Hippocampal CA1-Subiculum Synapses

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Roggenhofer, Elisabeth ^a,b   Fidzinski, Pawel ^a   Shor, Oded ^a   Behr, Joachim ^a,c  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

^c Ruppiner Kliniken GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; DOPAMINE 1 RECEPTOR; DOPAMINE 5 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; ENZYME ACTIVATION; FEMALE; HIPPOCAMPAL CA1 REGION; LONG TERM POTENTIATION; MALE; NERVE CELL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC POTENTIAL; RAT; SUBICULUM; SYNAPTIC TRANSMISSION; ANIMAL; ELECTROSTIMULATION; MEMBRANE POTENTIAL; METABOLISM; PHYSIOLOGY; PYRAMIDAL NERVE CELL; SYNAPSE;

RATTUS NORVEGICUS;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CALCIUM SIGNALING; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ELECTRIC STIMULATION; ENZYME ACTIVATION; FEMALE; LONG-TERM POTENTIATION; MALE; MEMBRANE POTENTIALS; PYRAMIDAL CELLS; RATS; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D5; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84876532649     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062520     Document Type: Article

References (81)

1. Lisman JE, Otmakhova NA, (2001) Storage, recall, and novelty detection of sequences by the hippocampus: elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine. Hippocampus 11: 551-568.
2. Hasselmo ME, Wyble BP, Wallenstein GV, (1996) Encoding and retrieval of episodic memories: role of cholinergic and GABAergic modulation in the hippocampus. Hippocampus 6: 693-708.
3. Hasselmo ME, Wyble BP, (1997) Free recall and recognition in a network model of the hippocampus: simulating effects of scopolamine on human memory function. Behav Brain Res 89: 1-34.
4. Naber PA, Witter MP, Lopes Silva FH, (2000) Networks of the hippocampal memory system of the rat. The pivotal role of the subiculum. Ann N Y Acad Sci 911: 392-403.
5. Chang EH, Huerta PT, (2012) Neurophysiological correlates of object recognition in the dorsal subiculum. Front Behav Neurosci 6: 46.
6. Deadwyler SA, Hampson RE, (2004) Differential but complementary mnemonic functions of the hippocampus and subiculum. Neuron 42: 465-476.
7. Burwell RD, (2000) The parahippocampal region: corticocortical connectivity. Ann N Y Acad Sci 911: 25-42.
8. Lisman JE, Grace AA, (2005) The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46: 703-713.
9. Ihalainen JA, Riekkinen P Jr, Feenstra MG, (1999) Comparison of dopamine and noradrenaline release in mouse prefrontal cortex, striatum and hippocampus using microdialysis. Neurosci Lett 277: 71-74.
10. Li S, Cullen WK, Anwyl R, Rowan MJ, (2003) Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat Neurosci 6: 526-531.
11. Wang SH, Redondo RL, Morris RG, (2010) Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory. Proc Natl Acad Sci U S A 107: 19537-19542.
12. Bliss TV, Collingridge GL, (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39.
13. Malenka RC, Nicoll RA, (1999) Long-term potentiation - a decade of progress? Science 285: 1870-1874.
14. Martin SJ, Grimwood PD, Morris RG, (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23: 649-711.
15. Otmakhova NA, Lisman JE, (1996) D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J Neurosci 16: 7478-7486.
16. Lemon N, Manahan-Vaughan D, (2006) Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J Neurosci 26: 7723-7729.
17. Huang YY, Kandel ER, (1995) 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 92: 2446-2450.
18. Matthies H, Becker A, Schroeder H, Kraus J, Hollt V, et al. (1997) Dopamine D1-deficient mutant mice do not express the late phase of hippocampal long-term potentiation. Neuroreport 8: 3533-3535.
19. Swanson-Park JL, Coussens CM, Mason-Parker SE, Raymond CR, Hargreaves EL, et al. (1999) A double dissociation within the hippocampus of dopamine D1/D5 receptor and beta-adrenergic receptor contributions to the persistence of long-term potentiation. Neuroscience 92: 485-497.
20. Jarsky T, Mady R, Kennedy B, Spruston N, (2008) Distribution of bursting neurons in the CA1 region and the subiculum of the rat hippocampus. J Comp Neurol 506: 535-547.
21. Taube JS, (1993) Electrophysiological properties of neurons in the rat subiculum in vitro. Exp Brain Res 96: 304-318.
22. Greene JR, Totterdell S, (1997) Morphology and distribution of electrophysiologically defined classes of pyramidal and nonpyramidal neurons in rat ventral subiculum in vitro. J Comp Neurol 380: 395-408.
23. Gigg J, Finch DM, O'Mara SM, (2000) Responses of rat subicular neurons to convergent stimulation of lateral entorhinal cortex and CA1 in vivo. Brain Res 884: 35-50.
24. van Welie I, Remme MW, van Hooft JA, Wadman WJ, (2006) Different levels of Ih determine distinct temporal integration in bursting and regular-spiking neurons in rat subiculum. J Physiol 576: 203-214.
25. O'Mara SM, Commins S, Anderson M, Gigg J, (2001) The subiculum: a review of form, physiology and function. Prog Neurobiol 64: 129-155.
26. Roggenhofer E, Fidzinski P, Bartsch J, Kurz F, Shor O, et al. (2010) Activation of dopamine D1/D5 receptors facilitates the induction of presynaptic long-term potentiation at hippocampal output synapses. Eur J Neurosci 32: 598-605.
27. Demers G, Griffin G, De Vroey G, Haywood JR, Zurlo J, et al. (2006) Animal research. Harmonization of animal care and use guidance. Science 312: 700-701.
28. Harris E, Stewart M, (2001) Intrinsic connectivity of the rat subiculum: II. Properties of synchronous spontaneous activity and a demonstration of multiple generator regions. J Comp Neurol 435: 506-518.
29. Knopp A, Kivi A, Wozny C, Heinemann U, Behr J, (2005) Cellular and network properties of the subiculum in the pilocarpine model of temporal lobe epilepsy. J Comp Neurol 483: 476-488.
30. Nicholls JG, Purves D, (1970) Monosynaptic chemical and electrical connexions between sensory and motor cells in the central nervous system of the leech. J Physiol 209: 647-667.
31. Berry MS, Pentreath VW, (1976) Criteria for distinguishing between monosynaptic and polysynaptic transmission. Brain Res 105: 1-20.
32. Miles R, Wong RK, (1987) Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol 388: 611-629.
33. Wozny C, Maier N, Schmitz D, Behr J, (2008) Two different forms of long-term potentiation at CA1-subiculum synapses. J Physiol 586: 2725-2734.
34. Lapointe V, Morin F, Ratte S, Croce A, Conquet F, et al. (2004) Synapse-specific mGluR1-dependent long-term potentiation in interneurones regulates mouse hippocampal inhibition. J Physiol 555: 125-135.
35. Stewart M, Wong RK, (1993) Intrinsic properties and evoked responses of guinea pig subicular neurons in vitro. J Neurophysiol 70: 232-245.
36. Staff NP, Jung HY, Thiagarajan T, Yao M, Spruston N, (2000) Resting and active properties of pyramidal neurons in subiculum and CA1 of rat hippocampus. J Neurophysiol 84: 2398-2408.
37. Vreugdenhil M, Hack SP, Draguhn A, Jefferys JG, (2002) Tetanus toxin induces long-term changes in excitation and inhibition in the rat hippocampal CA1 area. Neuroscience 114: 983-994.
38. Yang SN, (2000) Sustained enhancement of AMPA receptor- and NMDA receptor-mediated currents induced by dopamine D1/D5 receptor activation in the hippocampus: an essential role of postsynaptic Ca2+. Hippocampus 10: 57-63.
39. Mockett BG, Brooks WM, Tate WP, Abraham WC, (2004) Dopamine D1/D5 receptor activation fails to initiate an activity-independent late-phase LTP in rat hippocampus. Brain Res 1021: 92-100.
40. Beckstead RM, Wooten GF, Trugman JM, (1988) Distribution of D1 and D2 dopamine receptors in the basal ganglia of the cat determined by quantitative autoradiography. J Comp Neurol 268: 131-145.
41. Hjorth S, Carlsson A, (1988) In vivo receptor binding, neurochemical and functional studies with the dopamine D-1 receptor antagonist SCH23390. J Neural Transm 72: 83-97.
42. Hajos N, Ellender TJ, Zemankovics R, Mann EO, Exley R, et al. (2009) Maintaining network activity in submerged hippocampal slices: importance of oxygen supply. Eur J Neurosci 29: 319-327.
43. Maier N, Morris G, Johenning FW, Schmitz D, (2009) An approach for reliably investigating hippocampal sharp wave-ripples in vitro. PLoS One 4: e6925.
44. Zucker RS, Regehr WG, (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.
45. Faber DS, Korn H, (1991) Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys J 60: 1288-1294.
46. Bekkers JM, Stevens CF, (1990) Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 346: 724-729.
47. Malinow R, Tsien RW, (1990) Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346: 177-180.
48. Fremeau RT Jr, Duncan GE, Fornaretto MG, Dearry A, Gingrich JA, et al. (1991) Localization of D1 dopamine receptor mRNA in brain supports a role in cognitive, affective, and neuroendocrine aspects of dopaminergic neurotransmission. Proc Natl Acad Sci U S A 88: 3772-3776.
49. Ciliax BJ, Nash N, Heilman C, Sunahara R, Hartney A, et al. (2000) Dopamine D(5) receptor immunolocalization in rat and monkey brain. Synapse 37: 125-145.
50. Khan ZU, Gutierrez A, Martin R, Penafiel A, Rivera A, et al. (2000) Dopamine D5 receptors of rat and human brain. Neuroscience 100: 689-699.
51. Levey AI, Hersch SM, Rye DB, Sunahara RK, Niznik HB, et al. (1993) Localization of D1 and D2 dopamine receptors in brain with subtype-specific antibodies. Proc Natl Acad Sci U S A 90: 8861-8865.
52. Frey U, Schroeder H, Matthies H, (1990) Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices. Brain Res 522: 69-75.
53. Hernandez-Lopez S, Bargas J, Surmeier DJ, Reyes A, Galarraga E, (1997) D1 receptor activation enhances evoked discharge in neostriatal medium spiny neurons by modulating an L-type Ca2+ conductance. J Neurosci 17: 3334-3342.
54. Cepeda C, Buchwald NA, Levine MS, (1993) Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated. Proc Natl Acad Sci U S A 90: 9576-9580.
55. Cepeda C, Colwell CS, Itri JN, Chandler SH, Levine MS, (1998) Dopaminergic modulation of NMDA-induced whole cell currents in neostriatal neurons in slices: contribution of calcium conductances. J Neurophysiol 79: 82-94.
56. Surmeier DJ, Bargas J, Hemmings HC Jr, Nairn AC, Greengard P, (1995) Modulation of calcium currents by a D1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons. Neuron 14: 385-397.
57. Kitai ST, Surmeier DJ, (1993) Cholinergic and dopaminergic modulation of potassium conductances in neostriatal neurons. Adv Neurol 60: 40-52.
58. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG, (1998) Dopamine receptors: from structure to function. Physiol Rev 78: 189-225.
59. Blank T, Nijholt I, Teichert U, Kugler H, Behrsing H, et al. (1997) The phosphoprotein DARPP-32 mediates cAMP-dependent potentiation of striatal N-methyl-D-aspartate responses. Proc Natl Acad Sci U S A 94: 14859-14864.
60. Snyder GL, Fienberg AA, Huganir RL, Greengard P, (1998) A dopamine/D1 receptor/protein kinase A/dopamine- and cAMP-regulated phosphoprotein (Mr 32 kDa)/protein phosphatase-1 pathway regulates dephosphorylation of the NMDA receptor. J Neurosci 18: 10297-10303.
61. Levine MS, Altemus KL, Cepeda C, Cromwell HC, Crawford C, et al. (1996) Modulatory actions of dopamine on NMDA receptor-mediated responses are reduced in D1A-deficient mutant mice. J Neurosci 16: 5870-5882.
62. Raman IM, Tong G, Jahr CE, (1996) Beta-adrenergic regulation of synaptic NMDA receptors by cAMP-dependent protein kinase. Neuron 16: 415-421.
63. Cepeda C, Colwell CS, Itri JN, Gruen E, Levine MS, (1998) Dopaminergic modulation of early signs of excitotoxicity in visualized rat neostriatal neurons. Eur J Neurosci 10: 3491-3497.
64. Seamans JK, Durstewitz D, Christie BR, Stevens CF, Sejnowski TJ, (2001) Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. Proc Natl Acad Sci U S A 98: 301-306.
65. Wang J, O'Donnell P, (2001) D(1) dopamine receptors potentiate nmda-mediated excitability increase in layer V prefrontal cortical pyramidal neurons. Cereb Cortex 11: 452-462.
66. Lee FJ, Xue S, Pei L, Vukusic B, Chery N, et al. (2002) Dual regulation of NMDA receptor functions by direct protein-protein interactions with the dopamine D1 receptor. Cell 111: 219-230.
67. Varela JA, Hirsch SJ, Chapman D, Leverich LS, Greene RW, (2009) D1/D5 modulation of synaptic NMDA receptor currents. J Neurosci 29: 3109-3119.
68. Seamans JK, Yang CR, (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74: 1-58.
69. Lidow MS, Williams GV, Goldman-Rakic PS, (1998) The cerebral cortex: a case for a common site of action of antipsychotics. Trends Pharmacol Sci 19: 136-140.
70. Navakkode S, Sajikumar S, Frey JU, (2007) Synergistic requirements for the induction of dopaminergic D1/D5-receptor-mediated LTP in hippocampal slices of rat CA1 in vitro. Neuropharmacology 52: 1547-1554.
71. Wozny C, Maier N, Fidzinski P, Breustedt J, Behr J, et al. (2008) Differential cAMP signaling at hippocampal output synapses. J Neurosci 28: 14358-14362.
72. Behr J, Wozny C, Fidzinski P, Schmitz D, (2009) Synaptic plasticity in the subiculum. Prog Neurobiol 89: 334-342.
73. Wojtowicz AM, Fidzinski P, Heinemann U, Behr J, (2010) Beta-adrenergic receptor activation induces long-lasting potentiation in burst-spiking but not regular-spiking cells at CA1-subiculum synapses. Neuroscience 171: 367-372.
74. Maccaferri G, Toth K, McBain CJ, (1998) Target-specific expression of presynaptic mossy fiber plasticity. Science 279: 1368-1370.
75. Toth K, McBain CJ, (2000) Target-specific expression of pre- and postsynaptic mechanisms. J Physiol 525 Pt 1: 41-51.
76. Selig DK, Nicoll RA, Malenka RC, (1999) Hippocampal long-term potentiation preserves the fidelity of postsynaptic responses to presynaptic bursts. J Neurosci 19: 1236-1246.
77. Legault M, Wise RA, (2001) Novelty-evoked elevations of nucleus accumbens dopamine: dependence on impulse flow from the ventral subiculum and glutamatergic neurotransmission in the ventral tegmental area. Eur J Neurosci 13: 819-828.
78. Blaha CD, Yang CR, Floresco SB, Barr AM, Phillips AG, (1997) Stimulation of the ventral subiculum of the hippocampus evokes glutamate receptor-mediated changes in dopamine efflux in the rat nucleus accumbens. Eur J Neurosci 9: 902-911.
79. Taepavarapruk P, Floresco SB, Phillips AG, (2000) Hyperlocomotion and increased dopamine efflux in the rat nucleus accumbens evoked by electrical stimulation of the ventral subiculum: role of ionotropic glutamate and dopamine D1 receptors. Psychopharmacology (Berl) 151: 242-251.
80. Floresco SB, Todd CL, Grace AA, (2001) Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons. J Neurosci 21: 4915-4922.
81. Floresco SB, West AR, Ash B, Moore H, Grace AA, (2003) Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 6: 968-973.