Activation of muscarinic acetylcholine receptors induces a nitric oxide-dependent long-term depression in rat medial prefrontal cortex

Cerebral Cortex

Volumn 20, Issue 4, 2010, Pages 982-996

  Huang, Chiung Chun ^a   Hsu, Kuei Sen ^a,b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Glutamate; Long term depression; Medial prefrontal cortex; Muscarinic acetylcholine receptor; Nitric oxide

Indexed keywords

ATROPINE; CALCIUM; CARBACHOL; CYCLIC GMP DEPENDENT PROTEIN KINASE INHIBITOR; GUANYLATE CYCLASE INHIBITOR; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; MUSCARINIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; PHOSPHOLIPASE C; PIRENZEPINE; PROTEIN KINASE C;

ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVATION; LONG TERM DEPRESSION; MALE; NONHUMAN; PREFRONTAL CORTEX; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION; STIMULATION; SYNAPTIC TRANSMISSION;

ANIMALS; BIOPHYSICS; CARBACHOL; CHOLINERGIC AGONISTS; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGENTS; INOSITOL 1,4,5-TRISPHOSPHATE; LONG-TERM SYNAPTIC DEPRESSION; MALE; NEUROTRANSMITTER AGENTS; NITRIC OXIDE; PATCH-CLAMP TECHNIQUES; PREFRONTAL CORTEX; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, MUSCARINIC; SIGNAL TRANSDUCTION; TYPE C PHOSPHOLIPASES;

EID: 77949403304     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp161     Document Type: Article

References (57)

1. Bear MF, Abraham WC. 1996. Long-term depression in hippocampus. Annu Rev Neurosci. 19:437-462.
2. Bekkers JM, Stevens CF. 1990. Presynaptic mechanism for long-term potentiation in the hippocampus. Nature. 346:724-729.
3. Carroll RC, Beattie EC, von Zastrow M, Malenka RC. 2001. Role of AMPA receptor endocytosis in synaptic plasticity. Nat Rev Neurosci. 2:315-324.
4. Calabresi P, Gubellini P, Centonze D, Sancesario G, Morello M, Giorgi M, Pisani A, Bernardi G. 1999. A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression. J Neurosci. 19:2489-2499.
5. Daw MI, Chittajallu R, Bortolotto ZA, Dev KK, Duprat F, Henley JM, Collingridge GL, Isaac JT. 2000. PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses. Neuron. 28:873-886.
6. Day J, Damsma G, Fibiger HC. 1991. Cholinergic activity in the rat hippocampus, cortex and striatum correlates with locomotor activity: an in vivo microdialysis study. Pharmacol Biochem Behav. 38:723-729.
7. Dev KK, Nishimune A, Henley JM, Nakanishi S. 1999. The protein kinase Cα binding protein PICK1 interacts with short but not long form alternative splice variants of AMPA receptor subunits. Neuropharmacology. 38:635-644.
8. 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.
9. Everitt BJ, Robbins TW. 1997. Central cholinergic systems and cognition. Annu Rev Psychol. 48:649-684.
10. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B. 1995. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol. 48:184-188.
11. Gaykema RP, Luiten PG, Nyakas C, Traber J. 1990. Cortical projection patterns of the medial septum-diagonal band complex. J Comp Neurol. 293:103-124.
12. 2+-transport ATPase in rat skeletal muscle sarcoplasmic reticulum vesicles. Biochem Pharmacol. 37:978-981.
13. Grider JR. 1993. Interplay of VIP and nitric oxide in regulation of the descending relaxation phase of peristalsis.AmJ Physiol. 264:G334-G340.
14. Hayashi Y, Sekiyama N, Nakanishi S, Jane DE, Sunter DC, Birse EF, Udvarhelyi PM, Watkins JC. 1994. Analysis of agonist and antagonist activities of phenylglycine derivatives for different cloned metabotropic glutamate receptor subtypes. J Neurosci. 14:3370-3377.
15. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R. 2000. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science. 287:2262-2267.
16. Himmelheber AM, Sarter M, Bruno JP. 2000. Increases in cortical acetylcholine release during sustained attention performance in rats. Brain Res Cogn Brain Res. 9:313-325.
17. Houser CR, Crawford GD, Salvaterra PM, Vaughn JE. 1985. Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: a study of cholinergic neurons and synapses. J Comp Neurol. 234:17-34.
18. Huang CC, Hsu KS. 2006. Presynaptic mechanism underlying cAMP-induced synaptic potentiation in medial prefrontal cortex pyramidal neurons. Mol Pharmacol. 69:846-856.
19. Huang CC, Hsu KS. 2008. The role of NMDA receptors in regulating group II metabotropic glutamate receptor-mediated long-term depression in rat medial prefrontal cortex. Neuropharmacology. 54:1071-1078.
20. Huang CC, Yang PC, Lin HJ, Hsu KS. 2007. Repeated cocaine administration impairs group II metabotropic glutamate receptor-mediated long-term depression in rat medial prefrontal cortex. J Neurosci. 27:2958-2968.
21. Huang YY, Simpson E, Kellendonk C, Kandel ER. 2004. Genetic evidence for the bidirectional modulation of synaptic plasticity in the prefrontal cortex by D1 receptors. Proc Natl Acad Sci USA. 101:3236-3241.
22. Hulme EC, Birdsall NJ, Buckley NJ. 1990. Muscarinic receptor subtypes. Annu Rev Pharmacol Toxicol. 30:633-673.
23. Kemp JA, Foster AC, Leeson PD, Priestley T, Tridgett R, Iversen LL, Woodruff GN. 1988. 7-Chlorokynurenic acid is a selective antagonist at the glycine modulatory site of the N-methyl-D-aspartate receptor complex. Proc Natl Acad Sci USA. 85:6547-6550.
24. Kirkwood A, Rozas C, Kirkwood J, Perez F, Bear MF. 1999. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J Neurosci. 19:1599-1609.
25. Kreitzer AC, Regehr WG. 2001. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron. 29:717-727.
26. Lehmann J, Nagy JI, Atmadia S, Fibiger HC. 1980. The nucleus basalis magnocellularis: the origin of a cholinergic projection to the neocortex of the rat. Neuroscience. 5:1161-1174.
27. Lei S, Jackson MF, Jia Z, Roder J, Bai D, Orser BA, MacDonald JF. 2000. Cyclic GMP-dependent feedback inhibition of AMPA receptors is independent of PKG. Nat Neurosci. 3:559-565.
28. 2+ transients. Neuron. 15:407-415.
29. Lu W, Ziff EB. 2005. PICK1 interacts with ABP/GRIP to regulate AMPA receptor trafficking. Neuron. 47:407-421.
30. Lüscher C, Xia H, Beattie EC, Carroll RC, von Zastrow M, Malenka RC, Nicoll RA. 1999. Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron. 24:649-658.
31. Ma X, Suga N. 2005. Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex. Proc Natl Acad Sci USA. 102:9335-9340.
32. Malenka RC, Bear MF. 2004. LTP and LTD: an embarrassment of riches. Neuron. 44:5-21.
33. Manahan-Vaughan D, Braunewell KH. 1999. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc Natl Acad Sci USA. 96:8739-8744.
34. 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.
35. McCoy PA, McMahon LL. 2007. Muscarinic receptor dependent long-term depression in rat visual cortex is PKC independent but requires ERK1/2 activation and protein synthesis. J Neurophysiol. 98:1862-1870.
36. McGaughy J, Dalley JW, Morrison CH, Everitt BJ, Robbins TW. 2002. Selective behavioral and neurochemical effects of cholinergic lesions produced by intrabasalis infusions of 192 IgG-saporin on attentional performance in a five-choice serial reaction time task. J Neurosci. 22:1905-1913.
37. Mulkey RM, Malenka RC. 1992. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron. 9:967-975.
38. Otani S, Auclair N, Desce JM, Roisin MP, Crépel 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.
39. Otani S, Blond O, Desce JM, Crépel F. 1998. Dopamine facilitates long-term depression of glutamatergic transmission in rat prefrontal cortex. Neuroscience. 85:669-676.
40. Otani S, Daniel H, Takita M, Crépel 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.
41. Parikh V, Kozak R, Martinez V, Sarter M. 2007. Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron. 56:141-154.
42. Passetti F, Dalley JW, O'Connell MT, Everitt BJ, Robbins TW. 2000. Increased acetylcholine release in the rat medial prefrontal cortex during performance of a visual attentional task. Eur J Neurosci. 12:3051-3058.
43. 2+ release from cyclic ADP-ribose-sensitive stores. J Neurophysiol. 82:1569-1576.
44. 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.
45. Sarter M, Bruno JP. 1997. Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res Brain Res Rev. 23:28-46.
46. Satoh K, Fibiger HC. 1986. Cholinergic neurons of the laterodorsal tegmental nucleus: efferent and afferent connections. J Comp Neurol. 253:277-302.
47. 1 adrenergic receptors stimulates extracellular signal-regulated protein kinase and induces long-term depression at CA3-CA1 synapses in rat hippocampus. J Neurosci. 28:5350-5358.
48. Shibuki K, Okada D. 1991. Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature. 349:326-328.
49. Southan GJ, Szabó C. 1996. Selective pharmacological inhibition of distinct nitric oxide synthase isoforms. Biochem Pharmacol. 51:383-394.
50. Stevens CF, Wang Y. 1994. Changes in reliability of synaptic function as a mechanism for plasticity. Nature. 371:704-707.
51. Takita M, Izaki Y, Jay TM, Kaneko H, Suzuki SS. 1999. Induction of stable long-term depression in vivo in the hippocampal-prefrontal cortex pathway. Eur J Neurosci. 11:4145-4148.
52. Volk LJ, Pfeiffer BE, Gibson JR, Huber KM. 2007. Multiple Gq-coupled receptors converge on a common protein synthesis-dependent long-term depression that is affected in fragile X syndrome mental retardation. J Neurosci. 27:11624-11634.
53. Wang X, Robinson PJ. 1997. Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system. J Neurochem. 68:443-456.
54. White RE, Lee AB, Shcherbatko AD, Lincoln TM, Schonbrunn A, Armstrong DL. 1993. Potassium channel stimulation by natriuretic peptides through cGMP-dependent dephosphorylation. Nature. 361:263-266.
55. Wilson RI, Nicoll RA. 2001. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature. 410:588-592.
56. Wu J, Wang Y, Rowan MJ, Anwyl R. 1997. Evidence for involvement of the neuronal isoform of nitric oxide synthase during induction of long-term potentiation and long-term depression in the rat dentate gyrus in vitro. Neuroscience. 78:393-398.
57. Zucker RS. 1989. Short-term synaptic plasticity. Annu Rev Neurosci. 12:13-31.