Cholinergic interneurons suppress action potential initiation of medium spiny neurons in rat nucleus accumbens shell

Neuroscience

Volumn 236, Issue , 2013, Pages 332-344

  Ebihara, K ^a   Yamamoto, K ^a   Ueda, K ^a   Koshikawa, N ^a   Kobayashi, M ^a,b  

^a NIHON UNIVERSITY   (Japan)

^b RIKEN   (Japan)

Author keywords

Acetylcholine; Rheobase; Slowly inactivating potassium current; Spike firing

Indexed keywords

ACETYLCHOLINE; CARBACHOL; PIRENZEPINE;

ACETYLCHOLINE RELEASE; ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; FEMALE; INTERNEURON; MALE; MEDIUM SPINY NEURON; MEMBRANE STEADY POTENTIAL; NERVE CELL; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; NUCLEUS ACCUMBENS SHELL; PRIORITY JOURNAL; RAT; SPIKE; WHOLE CELL PATCH CLAMP; ANIMAL; CELL COMMUNICATION; METABOLISM; NUCLEUS ACCUMBENS; PATCH CLAMP; PHYSIOLOGY; WISTAR RAT;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; CELL COMMUNICATION; CHOLINERGIC NEURONS; FEMALE; INTERNEURONS; MALE; NUCLEUS ACCUMBENS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR;

EID: 84883010465     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.01.012     Document Type: Article

References (49)

1. Akaike A., Sasa M., Takaori S. Muscarinic inhibition as a dominant role in cholinergic regulation of transmission in the caudate nucleus. J Pharmacol Exp Ther 1988, 246:1129-1136.
2. + conductance in rat neostriatal neurons. Nature 1990, 344:240-242.
3. Bernardi G., Floris V., Marciani M.G., Morocutti C., Stanzione P. The action of acetylcholine and L-glutamic acid on rat caudate neurons. Brain Res. 1976, 114:134-138.
4. Calabresi P., Centonze D., Gubellini P., Pisani A., Bernardi G. Blockade of M2-like muscarinic receptors enhances long-term potentiation at corticostriatal synapses. Eur J Neurosci 1998, 10:3020-3023.
5. Calabresi P., Centonze D., Gubellini P., Pisani A., Bernardi G. Acetylcholine-mediated modulation of striatal function. Trends Neurosci 2000, 23:120-126.
6. A receptor function through a phospho-dependent endocytosis mechanism in nucleus accumbens. J Neurosci 2006, 26:2513-2521.
7. Contant C., Umbriaco D., Garcia S., Watkins K.C., Descarries L. Ultrastructural characterization of the acetylcholine innervation in adult rat neostriatum. Neuroscience 1996, 71:937-947.
8. 2 receptors in the nucleus accumbens in jaw movements of rats: a critical role of the shell. Eur J Pharmacol 1995, 286:41-47.
9. Di Chiara G. Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 2002, 137:75-114.
10. Dodt H.U., Misgeld U. Muscarinic slow excitation and muscarinic inhibition of synaptic transmission in the rat neostriatum. J Physiol 1986, 380:593-608.
11. English D.F., Ibanez-Sandoval O., Stark E., Tecuapetla F., Buzsáki G., Deisseroth K., Tepper J.M., Koos T. GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons. Nat Neurosci 2012, 15:123-130.
12. Gabel L.A., Nisenbaum E.S. Muscarinic receptors differentially modulate the persistent potassium current in striatal spiny projection neurons. J Neurophysiol 1999, 81:1418-1423.
13. Galarraga E., Hernandez-Lopez S., Reyes A., Miranda I., Bermudez-Rattoni F., Vilchis C., Bargas J. Cholinergic modulation of neostriatal output: a functional antagonism between different types of muscarinic receptors. J Neurosci 1999, 19:3629-3638.
14. Gertler T.S., Chan C.S., Surmeier D.J. Dichotomous anatomical properties of adult striatal medium spiny neurons. J Neurosci 2008, 28:10814-10824.
15. Gulley J.M., Doolen S., Zahniser N.R. Brief, repeated exposure to substrates down-regulates dopamine transporter function in Xenopus oocytes in vitro and rat dorsal striatum in vivo. J Neurochem 2002, 83:400-411.
16. 2 receptors increases spike firing of nucleus accumbens neurons via G-protein βγ subunits. J Neurosci 2003, 23:5079-5087.
17. Hsu K.S., Huang C.C., Gean P.W. Muscarinic depression of excitatory synaptic transmission mediated by the presynaptic M3 receptors in the rat neostriatum. Neurosci Lett 1995, 197:141-144.
18. Hsu K.S., Yang C.H., Huang C.C. Carbachol induces inward current in rat neostriatal neurons through a G-protein-coupled mechanism. Neurosci Lett 1997, 224:79-82.
19. 1-like muscarinic receptors. Neuroscience 1996, 73:751-760.
20. Kawaguchi Y. Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 1993, 13:4908-4923.
21. Kawaguchi Y., Wilson C.J., Augood S.J., Emson P.C. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 1995, 18:527-535.
22. Kitamura M., Koshikawa N., Yoneshige N., Cools A.R. Behavioural and neurochemical effects of cholinergic and dopaminergic agonists administered into the accumbal core and shell in rats. Neuropharmacology 1999, 38:1397-1407.
23. B autoreceptor-mediated suppression of GABA release in rat insular cortex. J Neurophysiol 2012, 107:1431-1442.
24. 2 agonists and antagonists injected into the nucleus accumbens and globus pallidus on jaw movements of rats. Eur J Pharmacol 1990, 182:375-380.
25. Lin J.Y., Chung K.K., de Castro D., Funk G.D., Lipski J. Effects of muscarinic acetylcholine receptor activation on membrane currents and intracellular messengers in medium spiny neurones of the rat striatum. Eur J Neurosci 2004, 20:1219-1230.
26. Ma Y.Y., Cepeda C., Chatta P., Franklin L., Evans C.J., Levine M.S. Regional and cell-type-specific effects of DAMGO on striatal D1 and D2 dopamine receptor-expressing medium-sized spiny neurons. ASN Neuro 2012, 4:e00077.
27. Nicola S.M. The nucleus accumbens as part of a basal ganglia action selection circuit. Psychopharmacology (Berl) 2007, 191:521-550.
28. Nicola S.M., Malenka R.C. Dopamine depresses excitatory and inhibitory synaptic transmission by distinct mechanisms in the nucleus accumbens. J Neurosci 1997, 17:5697-5710.
29. Nicola S.M., Malenka R.C. Modulation of synaptic transmission by dopamine and norepinephrine in ventral but not dorsal striatum. J Neurophysiol 1998, 79:1768-1776.
30. Nisenbaum E.S., Wilson C.J. Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J Neurosci 1995, 15:4449-4463.
31. Pakhotin P., Bracci E. Cholinergic interneurons control the excitatory input to the striatum. J Neurosci 2007, 27:391-400.
32. 2+ channels. J Neurophysiol 2005, 93:2507-2519.
33. Phelps P.E., Houser C.R., Vaughn J.E. Immunocytochemical localization of choline acetyltransferase within the rat neostriatum: a correlated light and electron microscopic study of cholinergic neurons and synapses. J Comp Neurol 1985, 238:286-307.
34. 3 receptors in islands of Calleja and shell of nucleus accumbens of the rat: opposite and synergistic functional interactions. Eur J Neurosci 1998, 10:1676-1686.
35. Rymar V.V., Sasseville R., Luk K.C., Sadikot A.F. Neurogenesis and stereological morphometry of calretinin-immunoreactive GABAergic interneurons of the neostriatum. J Comp Neurol 2004, 469:325-339.
36. Sharp T., Zetterstrom T., Ljungberg T., Ungerstedt U. A direct comparison of amphetamine-induced behaviours and regional brain dopamine release in the rat using intracerebral dialysis. Brain Res 1987, 401:322-330.
37. Shen W., Hamilton S.E., Nathanson N.M., Surmeier D.J. Cholinergic suppression of KCNQ channel currents enhances excitability of striatal medium spiny neurons. J Neurosci 2005, 25:7449-7458.
38. Stuber G.D., Hnasko T.S., Britt J.P., Edwards R.H., Bonci A. Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J Neurosci 2010, 30:8229-8233.
39. Sugita S., Uchimura N., Jiang Z.G., North R.A. Distinct muscarinic receptors inhibit release of γ-aminobutyric acid and excitatory amino acids in mammalian brain. Proc Natl Acad Sci U S A 1991, 88:2608-2611.
40. Takagi M., Yamamoto C. Suppressing action of cholinergic agents on synaptic transmissions in the corpus striatum of rats. Exp Neurol 1978, 62:433-443.
41. Takei H., Fujita S., Shirakawa T., Koshikawa N., Kobayashi M. Insulin facilitates repetitive spike firing in rat insular cortex via phosphoinositide 3-kinase but not mitogen activated protein kinase cascade. Neuroscience 2010, 170:1199-1208.
42. Taverna S., Ilijic E., Surmeier D.J. Recurrent collateral connections of striatal medium spiny neurons are disrupted in models of Parkinson's disease. J Neurosci 2008, 28:5504-5512.
43. Threlfell S., Cragg S.J. Dopamine signaling in dorsal versus ventral striatum: the dynamic role of cholinergic interneurons. Front Syst Neurosci 2011, 5:11.
44. Uchimura N., Cherubini E., North R.A. Inward rectification in rat nucleus accumbens neurons. J Neurophysiol 1989, 62:1280-1286.
45. Wilson C.J., Chang H.T., Kitai S.T. Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum. J Neurosci 1990, 10:508-519.
46. Windels F., Kiyatkin E.A. Modulatory action of acetylcholine on striatal neurons: microiontophoretic study in awake, unrestrained rats. Eur J Neurosci 2003, 17:613-622.
47. Witten I.B., Lin S.C., Brodsky M., Prakash R., Diester I., Anikeeva P., Gradinaru V., Ramakrishnan C., Deisseroth K. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 2010, 330:1677-1681.
48. Zhang L., Warren R.A. Muscarinic and nicotinic presynaptic modulation of EPSCs in the nucleus accumbens during postnatal development. J Neurophysiol 2002, 88:3315-3330.
49. Zhou F.M., Wilson C., Dani J.A. Muscarinic and nicotinic cholinergic mechanisms in the mesostriatal dopamine systems. Neuroscientist 2003, 9:23-36.