Multiple receptors coupled to phospholipase C gate long-term depression in visual cortex

Journal of Neuroscience

Volumn 25, Issue 49, 2005, Pages 11433-11443

  Choi, Se Young ^a   Chang, Jeff ^a   Jiang, Bin ^a   Seol, Geun Hee ^a   Min, Sun Seek ^a   Han, Jung Soo ^a   Shin, Hee Sup ^b   Gallagher, Michela ^a   Kirkwood, Alfredo ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b Korea Institute of Science and Technology   (South Korea)

Author keywords

Adrenergic; Cholinergic; Glutamatergic; LTD; Neuromodulation; Plasticity

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; GLUTAMATE RECEPTOR 5; INOSITOL 1,4,5 TRISPHOSPHATE; MUSCARINIC M1 RECEPTOR; PHOSPHOLIPASE C;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FOREBRAIN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RETINA; VISUAL CORTEX;

ANIMALS; ION CHANNEL GATING; LONG-TERM DEPRESSION (PHYSIOLOGY); MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHOLIPASE C; RATS; RATS, LONG-EVANS; RECEPTOR, MUSCARINIC M1; RECEPTORS, ADRENERGIC, ALPHA-1; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; VISUAL CORTEX;

EID: 30544455144     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4084-05.2005     Document Type: Article

References (86)

1. Allen CB, Celikel T, Feldman DE (2003) Long-term depression induced by sensory deprivation during cortical map plasticity in vivo. Nat Neurosci 6:291-299.
2. Baxter MG, Bucci DJ, Gorman LK, Wiley RG, Gallagher M (1995) Selective immunotoxic lesions of basal forebrain cholinergic cells: effects on learning and memory in rats. Behav Neurosci 109:714-722.
3. Bear MF, Abraham WC (1996) Long-term depression in hippocampus. Annu Rev Neurosci 19:437-462.
4. Bear MF, Rittenhouse CD (1999) Molecular basis for induction of ocular dominance plasticity. J Neurobiol 41:83-91.
5. Bear MF, Singer W (1986) Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320:172-176.
6. Blond O, Crepel F, Otani S (2002) Long-term potentiation in rat prefrontal slices facilitated by phased application of dopamine. Eur J Pharmacol 438:115-116.
7. Brocher S, Artola A, Singer W (1992) Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Res 573:27-36.
8. Castro-Alamancos MA, Donoghue JP, Connors BW (1995) Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex. J Neurosci 15:5324-5333.
9. Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461-472.
10. Cho K, Bashir Z (2002) Cooperation between mglu receptors: a depressing mechanism. Trends Neurosci 25:405-411.
11. Cho K, Kemp N, Noel J, Aggleton JP, Brown MW, Bashir ZI (2000) A new form of long-term depression in the perirhinal cortex. Nat Neurosci 3:150-156.
12. Cho K, Brown MW, Bashir ZI (2002) Mechanisms and physiological role of enhancement of mGlu5 receptor function by group II mGlu receptor activation in rat perirhinal cortex. J Physiol (Lond) 540:895-906.
13. Daw N, Gordon B, Fox K, Flavin H, Kirsch J, Beaver C, Ji Q, Reid S, Czepita D (1999) Injection of MK-801 affects ocular dominance shifts more than visual activity. J Neurophysiol 81:204-215.
14. Dodt H, Eder M, Frick A, Zieglgansberger W (1999) Precisely localized LTD in the neocortex revealed by infrared-guided laser stimulation. Science 286:110-113.
15. Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA 89:4363-4367.
16. Ego-Stengel V, Shulz DE, Haidarliu S, Sosnik R, Ahissar E (2001) Acetylcholine-dependent induction and ixpression of functional plasticity in the barrel cortex of the adult rat. J Neurophysiol 86:422-437.
17. Fitzjohn S, Bortolotto ZA, Palmer M, Doherty A, Ornstein P, Schoepp D, Kingston A, Lodge D, Collingridge G (1998) The potent mGlu receptor antagonist LY341495 identifies roles for both cloned and novel mGlu receptors in hippocampal synaptic plasticity. Neuropharmacology 37:1445-1458.
18. Fitzjohn S, Kingston A, Lodge D, Collingridge G (1999) DHPG-induced LTD in area CA1 of juvenile rat hippocampus; characterization and sensitivity to novel mGlu receptor antagonists. Neuropharmacology 38:1577-1583.
19. Fox K, Schlaggar BL, Glazewski S, O'Leary DDM (1996) Glutamate receptor blockade at cortical synapses disrupts development of thalamocortical and columnar organization in somatosensory cortex. Proc Natl Acad Sci USA 93:5584-5589.
20. Gu Q (2002) Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111:815-835.
21. Gu Q, Singer W (1995) Involvement of serotonin in developmental plasticity in kitten visual cortex. Eur J Neurosci 7:1146-1153.
22. Hannan AJ, Blakemore C, Katsnelson A, Vitalis T, Huber KM, Bear M, Roder J, Kim D, Shin HS, Kind PC (2001) PLC-beta1, activated via mGluRs, mediates activity-dependent differentiation in cerebral cortex. Nat Neurosci 4:282-288.
23. Haruta H, Kamishita T, Hicks TP, Takahashi MP, Tsumoto T (1994) Induction of LTD but not LTP through metabotropic glutamate receptors in visual cortex. NeuroReport 5:1829-1832.
24. 2+ dependency for triggering retrograde endocannabinoid signal. Neuron 45:257-268.
25. Hayashi ML, Choi SY, Rao BS, Jung HY, Lee HK, Zhang D, Chattarji S, Kirkwood A, Tonegawa S (2004) Altered cortical synaptic morphology and impaired memory consolidation in forebrain-specific dominant-negative PAK transgenic mice. Neuron 42:773-787.
26. Hohmann CF, Wilson L, Coyle JT (1991) Efferent and afferent connections of mouse sensory-motor cortex following cholinergic deafferentation at birth. Cereb Cortex 1:158-172.
27. Huber K, Kayser M, Bear M (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254-1257.
28. Huber KM, Sawtell NB, Bear MF (1998) Effects of the metabotropic glutamate receptor antagonist MCPG on phosphoinositide turnover and synaptic plasticity in visual cortex. J Neurosci 18:1-9.
29. Ikegaya Y, Ishizaka Y, Matsuki N (2002) BDNF attenuates hippocampal LTD via activation of phospholipase C: implications for a vertical shift in the frequency-response curve of synaptic plasticity. Eur J Neurosci 16:145-148.
30. Ireland DR, Abraham WC (2002) Group I mGluRs increase excitability of hippocampal CA1 pyramidal neurons by a PLC-independent mechanism. J Neurophysiol 88:107-116.
31. Iwasato T, Datwani A, Wolf AM, Nishiyama H, Taguchi Y, Tonegawa S, Knopfel T, Erzurumlu RS, Itohara S (2000) Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406:726-731.
32. Kandel E, O'Dell T (1992) Are adult learning mechanisms also used for development? Science 258:243-245.
33. Kandler K, Katz LC, Kauer JA (1998) Focal photolysis of caged glutamate produces long-term depression of hippocampal glutamate receptors. Nat Neurosci 1:119-123.
34. Karnowsky M, Roots L (1964) A "direct-coloring" thiocholine method for cholinesterase. J Histochem Cytochem 12:219-221.
35. Kasamatsu T, Pettigrew JD (1976) Depletion of brain catacholamines: failure of ocular dominance shift after monocular occlution in kittens. Science 194:206-209.
36. Kasamatsu T, Pettigrew JD (1979) Restoration of visual cortical plasticity by local microperfusion of norepinephrine. J Comp Neurol 185:163-182.
37. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
38. Kemp N, Bashir ZI (2001) Long-term depression: a cascade of induction and expression mechanisms. Prog Neurobiol 65:339-365.
39. Kilgard MP, Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalis activity. Science 279:1714-1718.
40. Kim D, Jun K, Lee S, Kang N, Min D, Kim Y, Ryu S, Suh P, Shin H (1997) Phospholipase C isozymes selectively couple to specific neurotransmitter receptors. Nature 389:290-293.
41. Kingston AE, Ornstein PL, Wright RA, Johnson BG, Mayne NG, Burnett JP, Belagaje R, Wu S, Schoepp DD (1998) LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology 37:1-12.
42. Kirkwood A (2000) Serotonergic control of developmental plasticity. Proc Natl Acad Sci USA 97:1951-1952.
43. Kirkwood A, Bear MF (1994) Homosynaptic long-term depression in the visual cortex. J Neurosci 14:3404-3412.
44. Kirkwood A, Rozas C, Kirkwood J, Perez F, Bear MF (1999) Modulation of long-term depression in visual cortex by acetylcholine and norepinephrine. J Neurosci 19:1599-1609.
45. Kleinschmidt A, Bear MF, Singer W (1987) Blockade of "NMDA" receptors disrupts experience-dependent modifications of kitten striate cortex. Science 238:355-358.
46. Kojic L, Dyck RH, Gu Q, Douglas RM, Matsuraba J, Cynader MS (2000) Columnar distribution of serotonin-dependent plasticity within kitten striate cortex. Proc Natl Acad Sci USA 97:1841-1844.
47. Kuczewski N, Aztiria E, Leanza G, Domenici L (2005) Selective cholinergic immunolesioning affects synaptic plasticity in developing visual cortex. Eur J Neurosci 21:1807-1814.
48. Lee HK, Kameyama K, Huganir RL, Bear MF (1998) NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 21:1151-1162.
49. Lee O, Lee CJ, Choi S (2002) Induction mechanisms for L-LTP at thalamic input synapses to the lateral amygdala: requirement of mGluR5 activation. NeuroReport 13:685-691.
50. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
51. Mannaioni G, Marino MJ, Valenti O, Traynelis SF, Conn PJ (2001) Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J Neurosci 21:5925-5934.
52. Manunta Y, Edeline JM (2004) Noradrenergic induction of selective plasticity in the frequency tuning of auditory cortex neurons. J Neurophysiol 92:1445-1463.
53. Massey PV, Bhabra G, Cho K, Brown MW, Bashir ZI (2001) Activation of muscarinic receptors induces protein synthesis-dependent long-lasting depression in the perirhinal cortex. Eur J Neurosci 14:145-152.
54. 2+ elevation induced by a brief BDNF application in rat visual cortex neurons. Neuro-Report 14:1481-1483.
55. Montgomery J, Madison D (2002) State-dependent heterogeneity in synaptic depression between pyramidal cell pairs. Neuron 33:765-777.
56. Mulkey RM, Malenka RC (1992) Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9:967-975.
57. Oliet SH, Malenka RC, Nicoll RA (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18:969-982.
58. Otani S, Auclair N, Desce JM, Roisin MP, Crepel F (1999) 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. J Neurosci 19:9788-9802.
59. Otani S, Daniel H, Takita M, Crepel F (2002) Long-term depression induced by postsynaptic group II metabotropic glutamate receptors linked to phospholipase C and intracellular calcium rises in rat prefrontal cortex. J Neurosci 22:3434-3444.
60. Palmer M, Irving A, Seabrook G, Jane D, Collingridge G (1997) The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus. Neuropharmacology 36:1517-1532.
61. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Perth, Australia: Academic Press Australia.
62. Philpot BD, Espinosa JS, Bear MF (2003) Evidence for altered NMDA receptor function as a basis for metaplasticity in visual cortex. J Neurosci 23:5583-5588.
63. Rao Y, Daw NW (2004) Layer variations of long-term depression in rat visual cortex. J Neurophysiol 92:2652-2658.
64. Renger JJ, Hartman KN, Tsuchimoto Y, Yokoi M, Nakanishi S, Hensch TK (2002) Experience-dependent plasticity without long-term depression by type 2 metabotropic glutamate receptors in developing visual cortex. Proc Natl Acad Sci USA 99:1041-1046.
65. Reyes-Harde M, Stanton PK (1998) Postsynaptic phospholipase C activity is required for the induction of homosynaptic long-term depression in rat hippocampus. Neurosci Lett 252:155-158.
66. Roberts EB, Meredith MA, Ramoa AS (1998) Suppression of NMDA receptor function using antisense DNA blocks ocular dominance plasticity while preserving visual responses. J Neurophysiol 80:1021-1032.
67. Rossner S, Schliebs R, Hartig W, Bigl V (1995) 192IGG-saporin-induced selective lesion of cholinergic basal forebrain system: neurochemical effects on cholinergic neurotransmission in rat cerebral cortex and hippocampus. Brain Res Bull 38:371-381.
68. Sachdev RN, Lu SM, Wiley RG, Ebner FF (1998) Role of the basal forebrain cholinergic projection in somatosensory cortical plasticity. J Neurophysiol 79:3216-3228.
69. Sanes JR, Lichtman JW (1999) Can molecules explain long-term potentiation? Nat Neurosci 2:597-604.
70. Sawtell NB, Huber KM, Roder JC, Bear MF (1999) Induction of NMDA receptor-dependent long-term depression in visual cortex does not require metabotropic glutamate receptors. J Neurophysiol 82:3594-3597.
71. Schliebs R, Rossner S, Bigl V (1996) Immunolesion by 192IgG-saporin of rat basal forebrain cholinergic system: a useful tool to produce cortical cholinergic dysfunction. Prog Brain Res 109:253-264.
72. Schnabel R, Kilpatrick I, Collingridge G (1999) An investigation into signal transduction mechanisms involved in DHPG-induced LTD in the CA1 region of the hippocampus. Neuropharmacology 38:1585-1596.
73. Selig DK, Lee H-K, Bear MF, Malenka RC (1995) Reexamination of the effects of MCPG on hippocampal LTP, LTD, and depotentiation. J Neurophysiol 74:1075-1082.
74. Shouval H, Bear M, Cooper L (2002) A unified model of NMDA receptor-dependent bidirectional synaptic plasticity. Proc Natl Acad Sci USA 99:10831-10836.
75. Shulz DE, Sosnik R, Ego V, Haidarliu S, Ahissar E (2000) A neuronal analogue of state-dependent learning. Nature 403:549-553.
76. Siciliano R, Fontanesi G, Casamenti F, Berardi N, Bagnoli P, Domenici L (1997) Postnatal development of functional properties of visual cortical cells in rats with excitotoxic lesions of basal forebrain cholinergic neurons. Vis Neurosci 14:11-123.
77. Siciliano R, Fornai F, Bonaccorsi I, Domenici L, Bagnoli P (1999) Cholinergic and noradrenergic afferents influence the functional properties of the postnatal visual cortex in rats. Vis Neurosci 16:1015-1028.
78. Singer W (1995) Development and plasticity of cortical processing architectures. Science 270:758-759.
79. Sjostrom PJ, Turrigiano GG, Nelson SB (2003) Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39:641-654.
80. Song S, Abbott L (2001) Cortical development and remapping through spike timing-dependent plasticity. Neuron 32:339-350.
81. Steele PM, Mauk MD (1999) Inhibitory control of LTP and LTD: stability of synapse strength. J Neurophysiol 81:1559-1566.
82. 2+ signalling: problems and pitfalls. Trends Pharmacol Sci 19:370-375.
83. 2+ influx in insulin-secreting cells. J Biol Chem 279:19396-19400.
84. Torii N, Kamishita T, Otsu Y, Tsumoto T (1995) An inhibitor for calcineurin, FK506, blocks induction of long-term depression in rat visual cortex. Neurosci Lett 185:1-4.
85. Yasuda H, Tsumoto T (1996) Long-term depression in rat visual cortex is associated with a lower rise of postsynaptic calcium than long-term potentiation. Neurosci Res 24:265-274.
86. Zhu XO, Waite PM (1998) Cholinergic depletion reduces plasticity of barrel field cortex. Cereb Cortex 8:63-72.