Synaptic muscarinic response types in hippocampal CA1 interneurons depend on different levels of presynaptic activity and different muscarinic receptor subtypes

Neuropharmacology

Volumn 73, Issue , 2013, Pages 160-173

  Bell, L Andrew ^a   Bell, Karen A ^a   McQuiston, A Rory ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Complex; Hippocampus; Interneuron; Medial septum diagonal band of Broca; Muscarinic synaptic potentials; Optogenetics

Indexed keywords

ACETYLCHOLINE; ATROPINE; INWARDLY RECTIFYING POTASSIUM CHANNEL; MUSCARINIC M1 RECEPTOR; MUSCARINIC M4 RECEPTOR; MUSCARINIC M5 RECEPTOR; MUSCARINIC RECEPTOR; PHYSOSTIGMINE;

ACETYLCHOLINE RELEASE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; DIAGONAL BAND OF BROCA; EXTRACELLULAR SPACE; HIPPOCAMPAL CA1 REGION; HYPERPOLARIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEPTUM PELLUCIDUM;

6,7-DINITROQUINOXALINE-2,3-DIONE; ACETYLCHOLINE; ACH; ACTION POTENTIAL; ANALYSIS OF VARIANCE; ANOVA; ANT; ANTAGONIST; AP; APV; BIC; BICUCULLINE; CA1; CHAT; CHOLINE ACETYLTRANSFERASE; CORNU AMMON 1; DIC; DIFFERENTIAL INTERFERENCE CONTRAST; DL-2-AMINO-5-PHOSPHONOPENTANOIC ACID; DNQX; EPSP; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; IPSP; LED; LIGHT EMITTING DIODE; MEDIAL SEPTUM/DIAGONAL BAND OF BROCA COMPLEX; MS/DBB; MUSCARINIC SYNAPTIC POTENTIALS; OPTOGENETICS; PAM; POSITIVE ALLOSTERIC MODULATOR; RAAV; RECOMBINANT ADENO-ASSOCIATED VIRUS; SC; SCHAFFER COLLATERAL; SEM; SLM; SO; SP; SR; STANDARD ERROR OF THE MEAN; STRATUM LACUNOSUM-MOLECULARE; STRATUM ORIENS; STRATUM PYRAMIDALE; STRATUM RADIATUM;

ACETYLCHOLINE; ANIMALS; ATROPINE; CA1 REGION, HIPPOCAMPAL; CHOLINESTERASE INHIBITORS; INTERNEURONS; MICE; MUSCARINIC ANTAGONISTS; PHYSOSTIGMINE; RECEPTORS, MUSCARINIC; SEPTUM OF BRAIN; SYNAPTIC POTENTIALS;

EID: 84885092331     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.05.026     Document Type: Article

References (57)

1. Atri, A., Sherman, S., Norman, K.A., Kirchhoff, B.A., Nicolas, M.M., Greicius, M.D., Cramer, S.C., Breiter, H.C., Hasselmo, M.E., Stern, CE., 2004. Blockade of central cholinergic receptors impairs new learning and increases proactive interference in a word paired-associate memory task. Behav. Neurosci. 118, 223-236. (Pubitemid 38222541)
2. Bell, K.A., Shim, H., Chen, C.-K., McQuiston, A.R., 2011. Nicotinic excitatory postsynaptic potentials in hippocampal CA1 interneurons are predominantly mediated by nicotinic receptors that contain a4 and b2 subunits. Neuropharmacology 61, 1379-1388.
3. Blokland, A., Honig, W., Raaijmakers, W.G., 1992. Effects of intra-hippocampal scopolamine injections in a repeated spatial acquisition task in the rat. Psychopharmacology 109, 373-376.
4. Bonner, T.I., 1989. New subtypes of muscarinic acetylcholine receptors. Trends Pharmacol. Sci. (Suppl:11-15). (Pubitemid 20004454)
5. Brazhnik, E.S., Fox, S.E., 1997. Intracellular recordings from medial septal neurons during hippocampal theta rhythm. Exp. Brain Res. Experimentelle Hirnforschung Expérimentation Cérébrale 114, 442-453. (Pubitemid 27214248)
6. Brazhnik, E.S., Fox, S.E., 1999. Action potentials and relations to the theta rhythm of medial septal neurons in vivo. Exp. Brain Res. Experimentelle Hirnforschung Expérimentation Cérébrale 127, 244-258. (Pubitemid 29349030)
7. Bridges, T.M., Phillip Kennedy, J., Noetzel, M.J., Breininger, M.L., Gentry, P.R., Conn, P.J., Lindsley, C.W., 2010. Chemical lead optimization of a pan Gq mAChR M1, M3, M5 positive allosteric modulator (PAM) lead. Part II: development of a potent and highly selective M1 PAM. Bioorg. Med. Chem. Lett. 20, 1972-1975.
8. Bridges, T.M., Marlo, J.E., Niswender, CM., Jones, C.K., Jadhav, S.B., Gentry, P.R., Plumley, H.C, Weaver, C.D., Conn, P.J., Lindsley, C.W., 2009. Discovery of the first highly m5-preferring muscarinic acetylcholine receptor ligand, an M5 positive allosteric modulator derived from a series of 5-Trifluoromethoxy N-Benzyl Isatins. J. Med. Chem. 52, 3445-3448.
9. Brown, D.A., 2010. Muscarinic acetylcholine receptors (mAChRs) in the nervous system: some functions and mechanisms. J. Mol. Neurosci. 41, 340-346.
10. Caccamo, A., Oddo, S., Billings, L.M., Green, K.N., Martinez-Coria, H., Fisher, A., LaFerla, F.M., 2006. M1 receptors play a central role in modulating AD-like pathology in transgenic mice. Neuron 49, 671-682. (Pubitemid 43290127)
11. Cea-del Rio, CA., Lawrence, J.J., Erdelyi, F., Szabo, G., McBain, C.J., 2011. Cholinergic modulation amplifies the intrinsic oscillatory properties of CA1 hippocampal cholecystokinin-positive interneurons. J. Physiol. (Lond) 589, 609-627.
12. Cea-del Rio, CA., Lawrence, J.J., Tricoire, L, Erdelyi, F., Szabo, G., McBain, C.J., 2010. M3 muscarinic acetylcholine receptor expression confers differential cholinergic modulation to Neurochemically distinct hippocampal basket cell subtypes. J. Neurosci. 30, 6011-6024.
13. Chiang, P.H., Yeh, W.C, Lee, C.T., Weng, J.Y., Huang, Y.Y., Lien, CC, 2010. M(1)-like muscarinic acetylcholine receptors regulate fast-spiking interneuron excitability in rat dentate gyrus. Neuroscience 169, 39-51.
14. Dasari, S., Gulledge, A.T., 2011. M1 and M4 receptors modulate hippocampal pyramidal neurons. J. Neurophysiol. 105, 779-792.
15. Descarries, L., Gisiger, V., Steriade, M., 1997. Diffuse transmission by acetylcholine in the CNS. Prog. Neurobiol. 53, 603-625. (Pubitemid 27489823)
16. Fornari, R.V., Moreira, K.M., Oliveira, M.G., 2000. Effects of the selective M1 muscarinic receptor antagonist dicyclomine on emotional memory. Learn Mem. 7, 287-292.
17. Freund, T.F., Buzsaki, G., 1996. Interneurons of the hippocampus. Hippocampus 6, 347-470. (Pubitemid 126682925)
18. Garber, J., 2011. Guide for the Care and Use of Laboratory Animals. National Academy Press.
19. Gu, Z., Yakel, J.L., 2011. Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity. Neuron 71, 155-165.
20. Gulledge, A.T., Kawaguchi, G.J., 2007. Phasic cholinergic signaling in the hippocampus: functional homology with the neocortex? Hippocampus 17, 327-332. (Pubitemid 46878814)
21. Hangya, B., Li, Y., Muller, R.U., Czurkó, A., 2010. Complementary spatial firing in place cell-interneuron pairs. J. Physiol. (Lond) 588, 4165-4175.
22. Hasselmo, M.E., 2006. The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 16, 710-715. (Pubitemid 44791918)
23. Hersch, S.M., Gutekunst, C.A., Rees, H.D., Heilman, C.J., Levey, A.I., 1994. Distribution of m1em4 muscarinic receptor proteins in the rat striatum: light and electron microscopic immunocytochemistry using subtype-specific antibodies. J. Neurosci. 14, 3351-3363. (Pubitemid 24139017)
24. Hulme, E.C., Birdsall, N.J., Buckley, N.J., 1990. Muscarinic receptor subtypes. Annu. Rev. Pharmacol. Toxicol. 30, 633-673. (Pubitemid 20139559)
25. King, C., Recce, M., O'Keefe, J., 1998. The rhythmicity of cells of the medial septum/diagonal band of Broca in the awake freely moving rat: relationships with behaviour and hippocampal theta. Eur. J. Neurosci. 10, 464-477. (Pubitemid 28325470)
26. Klausberger, T., Somogyi, P., 2008. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53-57. (Pubitemid 351956237)
27. Lawrence, J.J., Statland, J.M., Grinspan, Z.M., McBain, C.J., 2006. Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones. J. Physiol. (Lond) 570, 595-610.
28. Lee, M.-G., Hassani, O.K., Alonso, A., Jones, B.E., 2005. Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J. Neurosci. 25, 4365-4369. (Pubitemid 40628780)
29. Levey, A.I., Edmunds, S.M., Koliatsos, V., Wiley, R.G., Heilman, C.J., 1995. Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J. Neurosci. 15, 4077-4092.
30. Lin, J.Y., Lin, M.Z., Steinbach, P., Tsien, R.Y., 2009. Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys. J. 96, 1803-1814.
31. Manns, I.D., Alonso, A., Jones, B.E., 2000. Discharge properties of juxtacellularly labeled and immunohistochemically identified cholinergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J. Neurosci. 20, 1505-1518. (Pubitemid 30220429)
32. Manns, I.D., Alonso, A., Jones, B.E., 2003. Rhythmically discharging basal forebrain units comprise cholinergic, GABAergic, and putative glutamatergic cells. J. Neurophysiol. 89, 1057-1066. (Pubitemid 36206151)
33. Maurer, A.P., Cowen, S.L., Burke, S.N., Barnes, C.A., McNaughton, B.L., 2006. Phase precession in hippocampal interneurons showing strong functional coupling to individual pyramidal cells. J. Neurosci. 26, 13485-13492. (Pubitemid 46026480)
34. McMahon, L.L., Williams, J.H., Kauer, J.A., 1998. Functionally distinct groups of interneurons identified during rhythmic carbachol oscillations in hippocampus in vitro. J. Neurosci. 18, 5640-5651. (Pubitemid 28341344)
35. McQuiston, A.R., Madison, D.V., 1999a. Muscarinic receptor activity has multiple effects on the resting membrane potentials of CA1 hippocampal interneurons. J. Neurosci. 19, 5693-5702. (Pubitemid 29327906)
36. McQuiston, A.R., Madison, D.V., 1999b. Muscarinic receptor activity induces an afterdepolarization in a subpopulation of hippocampal CA1 interneurons. J. Neurosci. 19, 5703-5710. (Pubitemid 29327907)
37. Moscovitch, M., Nadel, L., Winocur, G., Gilboa, A., Rosenbaum, R.S., 2006. The cognitive neuroscience of remote episodic, semantic and spatial memory. Curr. Opin. Neurobiol. 16, 179-190.
38. Mrzljak, L., Levey, A.I., Goldman-Rakic, P.S., 1993. Association of m1 and m2 muscarinic receptor proteins with asymmetric synapses in the primate cerebral cortex: morphological evidence for cholinergic modulation of excitatory neurotransmission. Proc. Natl. Acad. Sci. USA 90, 5194-5198. (Pubitemid 23183004)
39. Nagode, D.A., Tang, A.-H., Karson, M.A., Klugmann, M., Alger, B.E., 2011. Optogenetic release of ACh induces rhythmic bursts of perisomatic IPSCs in hippocampus. PLoS ONE 6, e27691.
40. Parikh, V., Kozak, R., Martinez, V., Sarter, M., 2007. Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron 56, 141-154. (Pubitemid 47484179)
41. Parra, P., Gulyás, A.I., Miles, R., 1998. How many subtypes of inhibitory cells in the hippocampus? Neuron 20, 983-993. (Pubitemid 28247403)
42. Rouse, S.T., Hamilton, S.E., Potter, L.T., Nathanson, N.M., Conn, P.J., 2000. Muscarinic-induced modulation of potassium conductances is unchanged in mouse hip-pocampal pyramidal cells that lack functional M1 receptors. Neurosci. Lett. 278, 61-64. (Pubitemid 30009897)
43. Royer, S., Zemelman, B.V., Losonczy, A., Kim, J., Chance, F., Magee, J.C., Buzsáki, G., 2012. Control of Timing, Rate and Bursts of Hippocampal Place Cells by Dendritic and Somatic Inhibition. Nature Publishing Group.
44. Schnütgen, F., Doerflinger, N., Calléja, C., Wendling, O., Chambon, P., Ghyselinck, N.B., 2003. A directional strategy for monitoring Cre-mediated recombination at the cellular level in the mouse. Nat. Biotechnol. 21, 562-565. (Pubitemid 36532023)
45. Sheffler, D.J., Williams, R., Bridges, T.M., Xiang, Z., Kane, A.S., Byun, N.E., Jadhav, S., Mock, M.M., Zheng, F., Lewis, L.M., Jones, C.K., Niswender, C.M., Weaver, C.D., Lindsley, C.W., Conn, P.J., 2009. A novel selective muscarinic acetylcholine receptor subtype 1 antagonist reduces seizures without impairing hippocampus-dependent learning. Mol. Pharmacol. 76, 356-368.
46. Shirey, J.K., Xiang, Z., Orton, D., Brady, A.E., Johnson, K.A., Williams, R., Ayala, J.E., Rodriguez, A.L., Wess, J., Weaver, D., Niswender, C.M., Conn, P.J., 2008. An allosteric potentiator of M4 mAChR modulates hippocampal synaptic transmission. Nat. Chem. Biol. 4, 42-50. (Pubitemid 350273654)
47. Simon, A.P., Poindessous-Jazat, F., Dutar, P., Epelbaum, J., Bassant M-, H., 2006. Firing properties of anatomically identified neurons in the medial septum of anesthetized and unanesthetized restrained rats. J. Neurosci. 26, 9038-9046. (Pubitemid 44319395)
48. Soares, J.C.K., Fornari, R.V., Oliveira, M.G.M., 2006. Role of muscarinic M1 receptors in inhibitory avoidance and contextual fear conditioning. Neurobiol. Learn Mem. 86, 188-196. (Pubitemid 44287578)
49. Turrini, P., Casu, M.A., Wong, T.P., De Koninck, Y., Ribeiro-da-Silva, A., Cuello, A.C., 2001. Cholinergic nerve terminals establish classical synapses in the rat cerebral cortex: synaptic pattern and age-related atrophy. NSC 105, 277-285. (Pubitemid 32728112)
50. Umbriaco, D., Garcia, S., Beaulieu, C., Descarries, L., 1995. Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus 5, 605-620. (Pubitemid 26088292)
51. Umbriaco, D., Watkins, K.C., Descarries, L., Cozzari, C., Hartman, B.K., 1994. Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections. J. Comp. Neurol. 348, 351-373. (Pubitemid 24309899)
52. Vijayan, V.K., 1979. Distribution of cholinergic neurotransmitter enzymes in the hippocampus and the dentate gyrus of the adult and the developing mouse. NSC 4, 121-137. (Pubitemid 9111447)
53. Volpicelli, L.A., Levey, A.I., 2004. Muscarinic acetylcholine receptor subtypes in cerebral cortex and hippocampus. Prog. Brain Res. 145, 59-66. (Pubitemid 37442934)
54. Wall, S.J., Yasuda, R.P., Li, M., Ciesla, W., Wolfe, B.B., 1992. Differential regulation of subtypes m1-m5 of muscarinic receptors in forebrain by chronic atropine administration. J. Pharmacol. Exp. Ther. 262, 584-588.
55. Widmer, H., Ferrigan, L., Davies, C.H., Cobb, S.R., 2006. Evoked slow muscarinic acetylcholinergic synaptic potentials in rat hippocampal interneurons. Hippocampus 16, 617-628. (Pubitemid 44405264)
56. Zhang, H., Lin, S.-C., Nicolelis, M.A.L., 2010. Spatiotemporal coupling between hip-pocampal acetylcholine release and theta oscillations in vivo. J. Neurosci. 30, 13431-13440.
57. 2 muscarinic receptors. Neurosci. Lett. 494, 217-221.