Presynaptic muscarinic receptors reduce synaptic depression and facilitate its recovery at hippocampal GABAergic synapses

Cerebral Cortex

Volumn 24, Issue 7, 2014, Pages 1818-1831

  Gonzalez J C ^a,b   Lignani, G ^d,e   Maroto, M ^a,b   Baldelli, P ^d,e   Hernandez Guijo J M ^a,b,c  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO TEÓFILO HERNANDO   (Spain)

^c AUTONOMOUS UNIVERSITY OF MADRID   (Spain)

^d ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^e UNIVERSITY OF GENOA   (Italy)

Author keywords

hippocampal neurons; methacholine; muscarinic receptors; aminobutyric acidergic synapses

Indexed keywords

4 AMINOBUTYRIC ACID; METHACHOLINE; MUSCARINIC RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL; 2-AMINO-5-PHOSPHOPENTANOIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; AMINO ACID RECEPTOR BLOCKING AGENT; METHACHOLINE CHLORIDE; MUSCARINIC AGENT; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN; VALINE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEPTH STIMULATION; CALCIUM CURRENT; CELL DAMAGE; CONTROLLED STUDY; DOWN REGULATION; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; HIPPOCAMPUS; IN VITRO STUDY; NERVE CELL NETWORK; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; OSCILLATION; POSTSYNAPTIC INHIBITION; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; STEADY STATE; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP TECHNIQUE; ANALOGS AND DERIVATIVES; ANIMAL; ANIMAL EMBRYO; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; FEMALE; INHIBITORY POSTSYNAPTIC POTENTIAL; METABOLISM; PHYSIOLOGY; PREGNANCY; SPRAGUE DAWLEY RAT; SYNAPTOSOME; TIME;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GABAERGIC NEURONS; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIALS; METHACHOLINE CHLORIDE; MUSCARINIC AGONISTS; PREGNANCY; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, MUSCARINIC; SODIUM CHANNEL BLOCKERS; SYNAPSES; TETRODOTOXIN; TIME FACTORS; VALINE;

EID: 84902438551     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht032     Document Type: Article

References (87)

1. Abbott LF, Regehr WG. 2004. Synaptic computation. Nature. 431:796-803.
2. Adams PR, Brown DA, Constanti A. 1982. Pharmacological inhibition of the M-current. J Physiol. 332:223-262.
3. Allen TGJ, Brown DA. 1993. M2 muscarinic receptor-mediated inhibition of the Ca2+ current in rat magnocellular cholinergic basal forebrain neurones. J Physiol. 466:173-189.
4. Anglister L, Stiles JR, Salpeter MM. 1994. Acetylcholinesterase density and turnover number at frog neuromuscular junctions, with modeling of their role in synaptic function. Neuron. 12:783-794.
5. Anwar J, Spanevello RM, Thomé G, Stefanello N, Schmatz R, Gutierres J, Vieira J, Baldissarelli J, Carvalho FB, da Rosa MM et al. 2012. Effects of caffeic acid on behavioral parameters and on the activity of acetylcholinesterase in different tissues from adult rats. Pharmacol Biochem Behav. 103:386-394.
6. Arnaiz-Cot JJ, González JC, Sobrado M, Baldelli P, Carbone E, Hernandez-Guijo JM. 2008. Allosteric modulation of alpha7 nicotinic receptors selectively depolarizes hippocampal interneurons enhancing spontaneous GABAergic transmission. Eur J Neurosci. 27:1097-1110.
7. Aronica E, Iyer A, Zurolo E, Gorter JA. 2011. Ontogenetic modifications of neuronal excitability during brain maturation: developmental changes of neurotransmitter receptors. Epilepsia. 52:3-5.
8. Baldelli P, Forni PE, Carbone E. 2000. BDNF, NT-3 and NGF induce distinct new Ca2+ channel synthesis in developing hippocampal neurons. Eur J Neurosci. 12:4017-4032.
9. Baldelli P, Hernández-Guijo JM, Carabelli V, Carbone E. 2005. Brainderived neurotrophic factor enhances GABA release probability and nonuniform distribution of N- and P/Q-type channels on release sites of hippocampal inhibitory synapses. J Neurosci. 25:3358-3368.
10. Baldelli P, Novara M, Carabelli V, Hernández-Guijo JM, Carbone E. 2002. BDNF up-regulates evoked GABAergic transmission in developing hippocampal neurons by potentiating presynaptic N- and P/Q-type Ca2+ channel signalling. Eur J Neurosci. 16:2297-2310.
11. Bartos M, Vida I, Jonas P. 2007. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci. 8:45-56.
12. Beatty WW, Butters N, Janowsky DS. 1986. Patterns of memory failure after scopolamine treatment: implications for cholinergic hypotheses of dementia. Behav Neural Biol. 45:196-211.
13. Behrends JC, Bruggencate G. 1993. Cholinergic modulation of synaptic inhibition in the guinea pig hippocampus in vitro: excitation of GABAergic interneurons and inhibition of GABA-release. J Neurophysiol. 69:626-629.
14. Beier SM, Barish ME. 2000. Cholinergic stimulation enhances cytosolic calcium ion accumulation in mouse hippocampal CA1 pyramidal neurones during short action potential trains. J Physiol (Lond). 526:129-142.
15. Bekkers JM, Stevens CF. 1991. Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci USA. 88:7834-7838.
16. Benardo LS, Prince DA. 1982. Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res. 249:315-331.
17. Beutner D, Voets T, Neher E, Moser T. 2001. Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron. 29:681-690.
18. Blitzer RD, Gil O, Landau EM. 1990. Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci Lett. 119:207-210.
19. Bonner TI. 1989. New subtypes of muscarinic acetylcholine receptors. Trends Pharmacol Sci. 10(Suppl):11-15.
20. Brody DL, Yue DT. 2000. Relief of G-protein inhibition of calcium channels and short-term synaptic facilitation in cultured hippocampal neurons. J Neurosci. 20:889-898.
21. Callahan MJ, Kinsora JJ, Harbaugh RE, Reeder TM, Davis RE. 1993. Continuous ICV infusion of scopolamine impairs sustained attention of rhesus monkeys. Neurobiol Aging. 14:147-151.
22. Campbell V, Berrow NS, Fitzgerald EM, Brickley K, Dolphin AC. 1995. Inhibition of the interaction of G protein Go with calcium channels by the calcium channel β-subunit in rat neurones. J Physiol (Lond). 485:365-372.
23. Cole AE, Nicoll RA. 1983. Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science. 221:1299-1301.
24. Decker MW, McGaugh JL. 1991. The role of interactions between the cholinergic system and other neuromodulatory systems in learning and memory. Synapse. 7:151-168.
25. Delmas P, Abogadie FC, Dayell M, Haley JE, Milligan G, Caulfield MP, Brown DA, Buckley NJ. 1998. G-proteins and G-protein subunits mediating cholinergic inhibition of N-type calcium currents in sympathetic neurons. Eur J Neurosci. 10:1654-1666.
26. Drachman DA, Leavitt J. 1974. Human memory and the cholinergic system. A relationship to aging? Arch Neurol. 30:113-121.
27. Dutar P, Bassant MH, Senut MC, Lamour Y. 1995. The septohippocampal pathway: structure and function of a central cholinergic system. Physiol Rev. 75:393-427.
28. Fellous JM, Sejnowski TJ. 2000. Cholinergic induction of oscillations in the hippocampal slice in the slow (0.5-2 Hz), theta (5-12 Hz), and gamma (35-70 Hz) bands. Hippocampus. 10:187-197.
29. Fernández de Sevilla D, Buño W. 2010. The muscarinic long-term enhancement of NMDA and AMPA receptor-mediated transmission at Schaffer collateral synapses develop through different intracellular mechanisms. J Neurosci. 30:11032-11042.
30. Fibiger HC. 1991. Cholinergic mechanisms in learning, memory and dementia: a review of recent evidence. Trends Neurosci. 14:220-223.
31. Fisahn A, Pike FG, Buhl EH, Paulsen O. 1998. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature. 394:186-189.
32. Freund TF, Gulyás AI. 1997. Inhibitory control of GABAergic interneurons in the hippocampus. Can J Physiol Pharmacol. 75:479-487.
33. Fries P, Reynolds JH, Rorie AE, Desimone R. 2001. Modulation of oscillatory neuronal synchronization by selective visual attention. Science. 291:1560-1563.
34. Giessel AJ, Sabatini BL. 2010. M1 muscarinic receptors boost synaptic potentials and calcium influx in dendritic spines by inhibiting postsynaptic SK channels. Neuron. 68:936-947.
35. González JC, Albiñana E, García AG, Baldelli P, Hernández-Guijo JM. 2011. Presynaptic muscarinic receptor subtypes involved in the enhancement of spontaneous GABAergic postsynaptic currents in hippocampal neurons. Eur J Neurosci. 33:69-81.
36. González-Rubio JM, García de Diego AM, Egea J, Olivares R, Rojo J, Gandía L, García AG, Hernández-Guijo JM. 2006. Blockade of nicotinic receptors of bovine adrenal chromaffin cells by nanomolar concentrations of atropine. Eur J Pharmacol. 535:13-24.
37. Guerineau NC, Bossu JL, Gahwiler BH, Gerber U. 1995. Activation of a nonselective cationic conductance by methabotropic glutamatergic nd muscarinic agonists in CA3 pyramidal neurons of the rat hippocampus. J Neurosci. 15:4395-4407.
38. Gulyás AI, Hájos N, Freund TF. 1996. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci. 16:3397-3411.
39. Gupta A, Wang Y, Markram H. 2000. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science. 287:273-278.
40. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch Eur J Physiol. 391:85-100.
41. Hefft S, Kraushaar U, Geiger JR, Jonas P. 2002. Presynaptic short-term depression is maintained during regulation of transmitter release at a GABAergic synapse in rat hippocampus. J Physiol. 539:201-208.
42. Herlitze S, García DE, Mackie K, Hille B, Scheuer T, Catterall WA. 1996. Modulation of Ca2+ channels by G-protein βγ subunits. Nature. 380:258-262.
43. Hernández-Guijo JM, Gandía L, Lara B, García AG. 1998. Autocrine/ paracrine modulation of calcium channels in bovine chromaffin cells. Pflügers Arch Eur J Physiol. 437:104-113.
44. Higley MJ, Soler-Llavina GJ, Sabatini BL. 2009. Cholinergic modulation of multivesicular release regulates striatal synaptic potency and integration. Nature Neurosci. 12:1121-1128.
45. Howe AR, Surmeier DJ. 1995. Muscarinic receptors modulate N-, P-, and L-type Ca2+ currents in rat striatal neurons through parallel pathways. J Neurosci. 15:458-469.
46. Ikeda SR. 1996. Voltage-dependent modulation of N-type calcium channels by G-protein βγ subunits. Nature. 380:255-258.
47. Jensen K, Jensen MS, Lambert JD. 1999. Post-tetanic potentiation of GABAergic IPSCs in cultured rat hippocampal neurones. J Physiol (Lond). 519:71-84.
48. Jensen O, Idiart MA, Lisman JE. 1996. Physiologically realistic formation of autoassociative memory in networks with theta/ gamma oscillations: role of fast NMDA channels. Learn Mem. 3:243-256.
49. Jeong S, Wurster RD. 1997. Muscarinic receptor activation modulates Ca2+ channels in rat intracardiac neurons via a PTX- and voltagesensitive pathway. J Neurophysiol. 78:1476-1490.
50. Krnjevic K. 1993. Central cholinergic mechanisms and function. Prog Brain Res. 98:285-292.
51. Liu J, Evans MS, Lee JF. 2002. Presynaptic muscarinic M2 receptor mediated inhibition of N Type Ca2+ channels in cultured sphenopalatine ganglion: direct evidence for acetylcholine inhibition of cerebral nitrergic neurogenic vasodilation. J Pharmacol Exp Ther. 301:397-405.
52. Llinás R, Ribary U, Contreras D, Pedroarena C. 1998. The neuronal basis for consciousness. Philos Trans R Soc Lond B Biol Sci. 353:1841-1849.
53. Ma XH, Zhong P, Gu Z, Feng J, Yan Z. 2003. Muscarinic potentiation of GABA(A) receptor currents is gated by insulin signaling in the prefrontal cortex. J Neurosci. 23:1159-1168.
54. Madison DV, Lancaster B, Nicoll RA. 1987. Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci. 7:733-741.
55. Marchi M, Raiteri M. 1989. Interaction acetylcholine-glutamate in rat hippocampus: involvement of the two subtypes of M-2 muscarinic receptors. J Pharmacol Exp Ther. 248:1255-1260.
56. Markowska AL, Olton DS, Givens B. 1995. Cholinergic manipulations in the medial septal area: age-related effects on working memory and hippocampal electrophysiology. J Neurosci. 15:2063-2073.
57. Markram H, Segal M. 1990. Long-lasting facilitation of excitatory postsynaptic potentials in the rat hippocampus by acetylcholine. J Physiol. 427:381-393.
58. Marks B, McMahon HT. 1998. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr Biol. 8:740-749.
59. Mathie A, Bernheim L, Hille B. 1992. Inhibition of N- and L-type calcium channels by muscarinic receptor activation in rat sympathetic neurons. Neuron. 8:907-914.
60. McKinney M. 1993. Muscarinic receptor subtype-specific coupling to second messengers in neuronal systems. Prog Brain Res. 98:333-340.
61. McQuiston AR, Madison DV. 1999. Muscarinic receptor activity induces an afterdepolarization in a subpopulation of hippocampal CA1 interneurons. J Neurosci. 19:5703-5710.
62. Muller W, Connor JA. 1991. Cholinergic input uncouples Ca2+ changes from K+ conductance activation and amplifies intradendritic Ca2+ changes in hippocampal neurons. Neuron. 6:901-905.
63. Nair HK, Seravalli J, Arbuckle T, Quinn DM. 1994. Molecular recognition in acetylcholinesterase catalysis: free-energy correlations for substrate turnover and inhibition by trifluoro ketone transitionstate analogs. Biochemistry. 33:8566-8576.
64. Pang K, Williams MJ, Olton DS. 1993. Activation of the medial septal area attenuates LTP of the lateral perforant path and enhances heterosynaptic LTD of the medial perforant path in aged rats. Brain Res. 632:150-160.
65. Pavia J, de Ceballos ML, Sanchez de la Cuesta F. 1998. Alzheimer's disease: relationship between muscarinic cholinergic receptors, beta-amyloid and tau proteins. Fund Clin Pharmacol. 12:473-481.
66. Pitler TA, Alger BE. 1992. Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J Physiol. 450:127-142.
67. Pohorecki R, Head R, Domino EF. 1988. Effects of selected muscarinic cholinergic antagonists on [zH] acetylcholine release from rat hippocampal slices. J Pharmacol Exp Ther. 244:213-217.
68. Poncer JC, McKinney RA, Gahwiler BH, Thompson SM. 2000. Differential control of GABA release at synapses from distinct interneurons in rat hippocampus. J Physiol. 528:123-130.
69. Raiteri M, Leardi R, Marchi M. 1984. Heterogeneity of presynaptic muscarinic receptors regulating neurotransmitter release in the rat brain. J Pharmacol Exp Ther. 228:209-214.
70. Roldan G, Bolanos-Badillo E, Gonzalez-Sanchez H, Quirarte GL, Prado-Alcala RA. 1997. Selective M1 muscarinic receptor antagonists disrupt memory consolidation of inhibitory avoidance in rats. Neurosci Lett. 230:93-96.
71. Sahara Y, Westbrook GL. 1993. Modulation of calcium currents by a metabotropic glutamate receptor involves fast and slow kinetic components in cultured hippocampal neurons. J Neurosci. 13:3041-3050.
72. Salgado H, Bellay T, Nichols JA, Bose M, Martinolich L, Perrotti L, Atzori M. 2007. Muscarinic M2 and M1 receptors reduce GABA release by Ca2+ channel modulation through activation of PI3K/ Ca2+-independent and PLC/Ca2+-dependent PKC. J Neurophysiol. 98:952-965.
73. Sarter M, Parikh V. 2005. Choline transporters, cholinergic transmission, and cognition. Nat Rev Neurosci. 6:48-56.
74. Scanziani T, Gahwiler BH, Thompson SM. 1995. Presynaptic inhibition of excitatory synaptic transmission by muscarinic and metabotropic glutamate receptor activation in the hippocampus: are Ca2+ channels involved? Neuropharmacology. 34:1549-1557.
75. Schneggenburger R, Meyer AC, Neher E. 1999. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron. 23:399-409.
76. Seeger T, Alzheimer C. 2001. Muscarinic activation of inwardly rectifying K(+) conductance reduces EPSPs in rat hippocampal CA1 pyramidal cells. J Physiol. 535:383-396.
77. Stewart AE, Yan Z, Surmeier DJ, Foehring RC. 1999. Muscarine modulates Ca2+ channel currents in rat sensorimotor pyramidal cells via two distinct pathways. J Neurophysiol. 81:72-84.
78. Sutherland RJ, Whishaw IQ, Regehr JC. 1982. Cholinergic receptor blockade impairs spatial localization by use of distal cues in the rat. J Comp Physiol Psychol. 96:563-573.
79. Tai K, Bond SD, MacMillan HR, Baker NA, Holst MJ, McCammon JA. 2003. Finite element simulations of acetylcholine diffusion in neuromuscular junctions. Biophys J. 84:2234-2241.
80. Toselli M, Lux HD. 1989. GTP-binding proteins mediate acetylcholine inhibition of voltage dependent calcium channels in hippocampal neurons. Pflügers Arch Eur J Physiol. 413:319-321.
81. Traub RD, Bibbig A, Fisahn A, LeBeau FE, Whittington MA, Buhl EH. 2000. A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. Eur J Neurosci. 12:4093-4106.
82. Van der Zee EA, Luiten PGM. 1993. GABAergic neurons of the rat dorsal hippocampus expresses muscarinic acetylcholine receptors. Brain Res Bull. 32:601-609.
83. Whitehouse PJ. 1993. Cholinergic therapy in dementia. Acta Neurol Scand. 149:42-45.
84. Widmer H, Ferrigan L, Davies CH, Cobb SR. 2006. Evoked slow muscarinic acetylcholinergic synaptic potentials in rat hippocampal interneurons. Hippocampus. 16:617-628.
85. Williams S, Johnston D. 1990. Muscarinic depression of synaptic transmission at the hippocampal mossy fiber synapse. J Neurophysiol. 64:1089-1097.
86. Zhong P, Gu Z, Wang X, Jiang H, Feng J, Yan Z. 2003. Impaired modulation of GABAergic transmission by muscarinic receptors in a mouse transgenic model of Alzheimer's disease. J Biol Chem. 278:26888-29896.
87. Zucker RS, Regehr WG. 2002. Short-term synaptic plasticity. Annu Rev Physiol. 64:355-405.