Cholinergic-mediated IP3-receptor activation induces long-lasting synaptic enhancement in CA1 pyramidal neurons

Journal of Neuroscience

Volumn 28, Issue 6, 2008, Pages 1469-1478

  Fernández De Sevilla, David ^a   Núñez, Angel ^b   Borde, Michel ^a   Malinow, Roberto ^c   Buño, Washington ^a  

^a INSTITUTO CAJAL   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

AMPA trafficking; Ca2+ wave; Endoplasmic reticulum; Inositol; LTPIP3; Muscarinic

Indexed keywords

ACETYLCHOLINE; AMPA RECEPTOR; ATROPINE; CALCIUM ION; CHOLINERGIC RECEPTOR; GLUTAMIC ACID; INOSITOL 1,4,5 TRISPHOSPHATE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; CALCIUM; CHOLINERGIC RECEPTOR STIMULATING AGENT;

ANIMAL TISSUE; ARTICLE; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DENDRITE; ENDOPLASMIC RETICULUM; LEARNING; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SENSORY NERVE; SYNAPSE; ANIMAL; COMPARATIVE STUDY; DRUG EFFECT; DRUG POTENTIATION; FEMALE; MALE; METABOLISM; NERVE CELL; PHYSIOLOGY; WISTAR RAT;

ACETYLCHOLINE; ANIMALS; CALCIUM; CHOLINERGIC AGENTS; FEMALE; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; LONG-TERM POTENTIATION; MALE; NEURONS; PYRAMIDAL CELLS; RATS; RATS, WISTAR;

EID: 38949190948     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2723-07.2008     Document Type: Article

References (55)

1. Abe T, Sugihara H, Nawa H, Shigemoto R, Mizuno N, Nakanishi S (1992) Molecular characterization of a novel metabotropic glutamate receptor mGluR5 coupled to inositol phosphate/Ca2+ signal transduction. J Biol Chem 267:13361-13368.
2. Aigner TG (1995) Pharmacology of memory: cholinergic-glutamatergic interactions. Curr Opin Neurobiol 5:155-160.
3. Amenta F, Liu A, Giannella M, Pigini M, Tayebati SK, Zaccheo D (1995) Age-related changes in the density of muscarinic cholinergic M1 and M2 receptor subtypes in pyramidal neurons of the rat hippocampus. Eur J Histochem 39:107-116.
4. Ashby MC, Ibaraki K, Henley JM (2004) It's green outside: tracking cell surface proteins with pH-sensitive GFP. Trends Neurosci 27:257-261.
5. Auerbach JM, Segal M (1994) A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol 72:2034-2040.
6. Auerbach JM, Segal M (1996) Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol 492:479-493.
7. Bardo S, Cavazzini MG, Emptage N (2006) The role of the endoplasmic reticulum Ca2+ store in the plasticity of central neurons. Trends Pharmacol Sci 27:78-84.
8. Benke TA, Luthi A, Isaac JT, Collingridge GL (1998) Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393:793-797.
9. Blokland A (1995) Acetylcholine: a neurotransmitter for learning and memory? Brain Res Brain Res Rev 21:285-300.
10. Borde M, Cazalets JR, Buno W (1995) Activity-dependent response depression in rat hippocampal CA1 pyramidal neurons in vitro. J Neurophysiol 74:1714-1729.
11. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40:361-379.
12. Cabezas C, Buno W (2006) Distinct transmitter release properties determine differences in short-term plasticity at functional and silent synapses. J Neurophysiol 95:3024-3034.
13. Castillo PE, Schoch S, Schmitz F, Sudhof TC, Malenka RC (2002) RIM1alpha is required for presynaptic long-term potentiation. Nature 415:327-330.
14. Cohen AS, Raymond CR, Abraham WC (1998) Priming of long-term potentiation induced by activation of metabotropic glutamate receptors coupled to phospholipase C. Hippocampus 8:160-170.
15. Dudar JD (1977) The role of the septal nuclei in the release of acetyl-choline from the rabbit cerebral cortex and dorsal hippocampus and the effect of atropine. Brain Res 129:237-246.
16. Dutar P, Nicoll RA (1988) Classification of muscarinic responses in hippocampus in terms of receptor subtypes and second-messenger systems: electrophysiological studies in vitro. J Neurosci 8:4214-4224.
17. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511-525.
18. Fernandez de Sevilla D, Buno W (2003) Presynaptic inhibition of Schaffer collateral synapses by stimulation of hippocampal cholinergic afferent fibres. Eur J Neurosci 17:555-558.
19. Fernandez de Sevilla D, Cabezas C, de Prada AN, Sanchez-Jimenez A, Buno W (2002) Selective muscarinic regulation of functional glutamatergic Schaffer collateral synapses in rat CA1 pyramidal neurons. J Physiol (Lond) 545:51-63.
20. Frotscher M, Leranth C (1985) Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J Comp Neurol 239:237-246.
21. Frotscher M, Vida I, Bender R (2000) Evidence for the existence of non-GABAergic, cholinergic interneurons in the rodent hippocampus. Neuroscience 96:27-31.
22. Gaztelu JM, Buno Jr W (1982) Septo-hippocampal relationships during EEG theta rhythm. Electroencephalogr Clin Neurophysiol 54:375-387.
23. Gogolak G, Stumpf C, Petsche H, Sterc J (1968) The firing pattern of septal neurons and the form of the hippocampal theta wave. Brain Res 7:201-207.
24. Hasselmo ME (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3:351-359.
25. Hoffman DA, Sprengel R, Sakmann B (2002) Molecular dissection of hippocampal theta-burst pairing potentiation. Proc Natl Acad Sci USA 99:7740-7745.
26. Huerta PT, Lisman JE (1995) Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 15:1053-1063.
27. 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.
28. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26:2000-2009.
29. Levey AI, Edmunds SM, Koliatsos V, Wiley RG, Heilman CJ (1995) Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J Neurosci 15:4077-4092.
30. Lin JW, Ju W, Foster K, Lee SH, Ahmadian G, Wyszynski M, Wang YT, Sheng M (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat Neurosci 3:1282-1290.
31. Lissin DV, Carroll RC, Nicoll RA, Malenka RC, von Zastrow M (1999) Rapid, activation-induced redistribution of ionotropic glutamate receptors in cultured hippocampal neurons. J Neurosci 19:1263-1272.
32. Mak DO, McBride S, Foskett JK (2001) Regulation by Ca2+ and inositol 1,4,5-trisphosphate (InsP3) of single recombinant type 3 InsP3 receptor channels. Ca2+ activation uniquely distinguishes types 1 and 3 insp3 receptors. J Gen Physiol 117:435-446.
33. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
34. Malenka RC, Kauer JA, Perkel DJ, Nicoll RA (1989) The impact of postsynaptic calcium on synaptic transmission-its role in long-term potentiation. Trends Neurosci 12:444-450.
35. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
36. Markram H, Segal M (1990) Acetylcholine potentiates responses to N-methyl-D-aspartate in the rat hippocampus. Neurosci Lett 113:62-65.
37. Markram H, Helm PJ, Sakmann B (1995) Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons. J Physiol 485:1-20.
38. Nishizaki T, Mori M (1998) Diverse signal transduction pathways mediated by endogenous P2 receptors in cultured rat cerebral cortical neurons. J Neurophysiol 79:2513-2521.
39. Oertner TG, Sabatini BL, Nimchinsky EA, Svoboda K (2002) Facilitation at single synapses probed with optical quantal analysis. Nat Neurosci 5:657-664.
40. Ovsepian SV, Anwyl R, Rowan MJ (2004) Endogenous acetylcholine lowers the threshold for long-term potentiation induction in the CA1 area through muscarinic receptor activation: in vivo study. Eur J Neurosci 20:1267-1275.
41. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. New York: Academic.
42. Power JM, Sah P (2002) Nuclear calcium signaling evoked by cholinergic stimulation in hippocampal CA1 pyramidal neurons. J Neurosci 22:3454-3462.
43. Qian J, Saggau P (1997) Presynaptic inhibition of synaptic transmission in the rat hippocampus by activation of muscarinic receptors: involvement of presynaptic calcium influx. Br J Pharmacol 122:511-519.
44. Ramón y Cajal S (1891) Significación fisiológica de las expansions protoplásmicas y nerviosas de la sustancia gris. Revista de Ciencias Médicas de Barcelona 22:23.
45. Rose CR, Konnerth A (2001) Stores not just for storage. intracellular calcium release and synaptic plasticity. Neuron 31:519-522.
46. Rovira C, Ben-Ari Y, Cherubini E (1983) Dual cholinergic modulation of hippocampal somatic and dendritic field potentials by the septohippocampal pathway. Exp Brain Res 49:151-155.
47. Scheiderer CL, McCutchen E, Thacker EE, Kolasa K, Ward MK, Parsons D, Harrell LE, Dobrunz LE, McMahon LL (2006) Sympathetic sprouting drives hippocampal cholinergic reinnervation that prevents loss of a muscarinic receptor-dependent long-term depression at CA3-CA1 synapses. J Neurosci 26:3745-3756.
48. 2+ release channels in rat brain. J Neurosci 13:3051-3063.
49. Shinoe T, Matsui M, Taketo MM, Manabe T (2005) Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 25:11194-11200.
50. Song I, Huganir RL (2002) Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25:578-588.
51. Spacek J, Harris KM (1997) Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J Neurosci 17:190-203.
52. Triller A, Choquet D (2005) Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move! Trends Neurosci 28:133-139.
53. Valentino RJ, Dingledine R (1981) Presynaptic inhibitory effect of acetylcholine in the hippocampus. J Neurosci 1:784-792.
54. Zenchenko KI, Kokoz YM, Ivanov VT, Ziganshin RH, Vinogradova OS (2000) State-dependent effects of some neuropeptides and neurotransmitters on neuronal activity of the medial septal area in brain slices of the ground squirrel, Citellus undulatus. Neuroscience 96:791-805.
55. Zucker RS (1999) Calcium- and activity-dependent synaptic plasticity. Curr Opin Neurobiol 9:305-313.