Modulation of direct pathway striatal projection neurons by muscarinic M4-type receptors

Neuropharmacology

Volumn 89, Issue , 2015, Pages 232-244

  Hernández Flores, Teresa ^a   Hernández González, Omar ^a   Pérez Ramírez, María B ^a   Lara González, Esther ^a   Arias García, Mario A ^a   Duhne, Mariana ^a   Pérez Burgos, Azucena ^a   Prieto, G Aleph ^a   Figueroa, Alejandra ^a   Galarraga, Elvira ^a   Bargas, José ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

Acetylcholine; CaV1 Ca2+ channels; Excitability; Striatal projection neurons; Striatum

Indexed keywords

DOPAMINE 1 RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; MUSCARINIC M1 RECEPTOR; MUSCARINIC M4 RECEPTOR; NICARDIPINE; SNAKE VENOM; VOLTAGE GATED CALCIUM CHANNEL; ACETYLCHOLINE; CALCIUM CHANNEL BLOCKING AGENT; DOPAMINE; DOPAMINE 2 RECEPTOR; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CELL ACTIVATION; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; INTERNEURON; MALE; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRIATAL PROJECTION NEURON; SYNAPTIC TRANSMISSION; ANIMAL; CELL CULTURE; CORPUS STRIATUM; CYTOLOGY; DRUG EFFECTS; GENETICS; IN VITRO STUDY; MEMBRANE POTENTIAL; METABOLISM; NERVE TRACT; PHYSIOLOGY; TRANSGENIC MOUSE;

ACETYLCHOLINE; ANIMALS; CALCIUM CHANNEL BLOCKERS; CELLS, CULTURED; CORPUS STRIATUM; DOPAMINE; IN VITRO TECHNIQUES; MALE; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; NEURAL PATHWAYS; NEURONS; NICARDIPINE; RECEPTOR, MUSCARINIC M4; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; SODIUM CHANNEL BLOCKERS; TETRODOTOXIN;

EID: 84922335511     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.09.028     Document Type: Article

References (84)

1. R.L. Albin, A.B. Young, and J.B. Penney The functional anatomy of basal ganglia disorders Trends. Neurosci. 12 1989 366 375 10.1016/0166-2236(89)90074-X
2. T. Aosaki, M. Miura, T. Suzuki, K. Nishimura, and M. Masuda Acetylcholine-dopamine balance hypothesis in the striatum: an update Geriatr. Gerontol. Int. 1 2010 148 157 10.1111/j.1447-0594.2010.00588.x
3. M.A. Arias-García, D. Tapia, E. Flores-Barrera, J.E. Perez-Ortega, J. Bargas, and E. Galarraga Duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currents Front. Syst. Neurosci. 7 63 2013 10.3389/fnsys.2013.00063
4. 2+ currents in acutely-isolated, adult rat neostriatal neurons J. Neurosci. 14 1994 6667 6686
5. J. Barral, E. Galarraga, D. Tapia, E. Flores-Barrera, A. Reyes, and J. Bargas Dopaminergic modulation of spiny neurons in the turtle striatum Cell. Mol. Neurobiol. 30 2010 743 750 10.1007/s10571-010-9499-7
6. C. Bertram, L. Dahan, L.W. Boorman, S. Harris, N. Vautrelle, M. Leriche, P. Redgrave, and P.G. Overton Cortical regulation of dopaminergic neurons: role of the midbrain superior colliculus J. Neurophysiol. 111 2014 755 767 10.1152/jn.00329.2013
7. K.N. Bradley Muscarinic toxins from the green mamba Pharmacol. Ther. 85 2000 87 109 10.1016/S0163-7258(99)00064-9
8. J.M. Burkhardt, X. Jin, and R.M. Costa Dissociable effects of dopamine on neuronal firing rate and synchrony in the dorsal striatum Front. Integr. Neurosci. 3 28 2009 10.3389/neuro.07.028.2009
9. L. Carrillo-Reid, F. Tecuapetla, D. Tapia, A. Hernández-Cruz, E. Galarraga, R. Drucker-Colin, and J. Bargas Encoding network states by striatal cell assemblies J. Neurophysiol. 99 2008 1435 1450 10.1152/jn.01131.2007
10. L. Carrillo-Reid, F. Tecuapetla, O. Ibáñez-Sandoval, A. Hernández-Cruz, E. Galarraga, and J. Bargas Activation of the cholinergic system endows compositional properties to striatal cell assemblies J. Neurophysiol. 101 2009 737 749 10.1152/jn.90975.2008
11. L. Carrillo-Reid, F. Tecuapetla, N. Vautrelle, A. Hernández, R. Vergara, E. Galarraga, and J. Bargas Muscarinic enhancement of persistent sodium current synchronizes striatal medium spiny neurons J. Neurophysiol. 102 2009 682 690 10.1152/jn.00134.2009
12. L. Carrillo-Reid, S. Hernández-López, D. Tapia, E. Galarraga, and J. Bargas Dopaminergic modulation of the striatal microcircuit: receptor specific configuration of cell assemblies J. Neurosci. 31 2011 14972 14983 10.1523/JNEUROSCI.3226-11.2011
13. C. Contant, D. Umbriaco, S. Garcia, K.C. Watkins, and L. Descarries Ultrastructural characterization of the acetylcholine innervation in adult rat neostriatum Neuroscience 71 1996 937 947 10.1016/0306-4522(95)00507-2
14. R.L. Cowan, and C.J. Wilson Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex J. Neurophysiol. 71 1994 17 32
15. D. Dautan, I. Huerta-Ocampo, I.B. Witten, K. Deisseroth, J.P. Bolam, T. Gerdjikov, and J. Mena-Segovia A major external source of cholinergic innervation of the striatum and nucleus accumbens originates in the brainstem J. Neurosci. 34 2014 4509 4518 10.1523/JNEUROSCI.5071-13.2014
16. V. de Lafuente, and R. Romo Dopaminergic activity coincides with stimulus detection by the frontal lobe Neuroscience 218 2012 181 184 10.1016/j.neuroscience.2012.05.026
17. M.R. DeLong Primate models of movement disorders of basal ganglia origin Trends Neurosci. 13 1990 281 285 10.1016/0166-2236(90)90110-V
18. 4 autoreceptor function in striatal cholinergic interneurons following dopamine depletion Nat. Neurosci. 9 2006 832 842 10.1038/nn1700
19. J.B. Ding, J.N. Guzman, J.D. Peterson, J.A. Goldberg, and D.J. Surmeier Thalamic gating of corticostriatal signaling by cholinergic interneurons Neuron 67 2010 294 307 10.1016/j.neuron.2010.06.017
20. G.,J. Digby, J.K. Shirey, and P.J. Conn Allosteric activators of muscarinic receptors as novel approaches for treatment of CNS disorders Mol. Biosyst. 6 2010 1345 1354 10.1039/c002938f
21. N.M. Doig, J. Moss, and J.P. Bolam Cortical and thalamic innervation of direct and indirect pathway medium-sized spiny neurons in mouse striatum J. Neurosci. 30 2010 14610 14618 10.1523/JNEUROSCI.1623-10.2010
22. V. Dolezal, and S. Tucek Calcium channels involved in the inhibition of acetylcholine release by presynaptic muscarinic receptors in rat striatum Br. J. Pharmacol. 127 1999 1627 1632 10.1038/sj.bjp.0702721
23. J. Ericsson, M. Stephenson-Jones, J. Pérez-Fernández, B. Robertson, G. Silberberg, and S. Grillner Dopamine differentially modulates the excitability of striatal neurons of the direct and indirect pathways in lamprey J. Neurosci. 33 2013 8045 8054 10.1523/JNEUROSCI.5881-12.2013
24. A. Figueroa, E. Galarraga, and J. Bargas Muscarinic receptors involved in the subthreshold cholinergic actions of neostriatal spiny neurons Synapse 46 2002 215 223 10.1002/syn.10114
25. E. Flores-Barrera, B.J. Vizcarra-Chacón, D. Tapia, J. Bargas, and E. Galarraga Different corticostriatal integration in spiny projection neurons from direct and indirect pathways Front. Syst. Neurosci. 4 15 2010 10.3389/fnsys.2010.00015
26. E. Flores-Barrera, B.J. Vizcarra-Chacón, J. Bargas, D. Tapia, and E. Galarraga Dopaminergic modulation of corticostriatal responses in medium spiny projection neurons from direct and indirect pathways Front. Syst. Neurosci. 5 15 2011 10.3389/fnsys.2011.00015
27. 1 muscarinic receptor using 125I-Met35-oxidized muscarinic toxin 7 Mol. Pharmacol. 69 2006 1641 1651 10.1124/mol.105.020883
28. 2+ conductance Neuroreport 8 1997 2183 2186
29. E. Galarraga, S. Hernández-López, A. Reyes, I. Miranda, F. Bermudez-Rattoni, C. Vilchis, and J. Bargas Cholinergic modulation of neostriatal output: a functional antagonism between different types of muscarinic receptors J. Neurosci. 19 1999 3629 3638
30. C.R. Gerfen, and D.J. Surmeier Modulation of striatal projection systems by dopamine Annu. Rev. Neurosci. 34 2011 441 466 10.1146/annurev-neuro-061010-113641
31. rd Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study Brain Res. 460 1988 161 167 10.1016/0006-8993(88)91217-6
32. J.A. Goldberg, J.B. Ding, and D.J. Surmeier Muscarinic modulation of striatal function and circuitry Handb. Exp. Pharmacol. 208 2012 223 241 10.1007/978-3-642-23274-9-10
33. E. Hernández-Echeagaray, E. Galarraga, and J. Bargas 3-α-chloro-imperialine, a potent blocker of cholinergic presynaptic modulation of glutamatergic afferents in the rat neostriatum Neuropharmacology 37 1998 1493 1502 10.1016/S0028-3908(98)00131-2
34. 2A receptors in striatal projection neurons Purinergic Signal. 10 2014 269 281 10.1007/s11302-013-9386-z
35. 2+ conductance J. Neurosci. 17 1997 3334 3342
36. 3-calcineurin-signaling cascade J. Neurosci. 20 2000 8987 8995
37. M.J. Higley, G.J. Soler-Llavina, and B.L. Sabatini Cholinergic modulation of multivesicular release regulates striatal synaptic potency and integration Nat. Neurosci. 12 2009 1121 1128 10.1038/nn.2368
38. 2+ currents in rat striatal neurons through parallel pathways J. Neurosci. 15 1995 458 469
39. 2 dopamine and m4 muscarinic acetylcholine receptor proteins in identified striatonigral neurons Synapse 27 1997 357 366 doi:10.1002/(SICI)1098-2396(199712)27:4<357::AID-SYN9>3.0.CO;2-B
40. O. Jáidar, L. Carrillo-Reid, A. Hernández, R. Drucker-Colín, J. Bargas, and A. Hernández-Cruz Dynamics of the Parkinsonian striatal microcircuit: entrainment into a dominant network state J. Neurosci. 30 2010 11326 11336 10.1523/JNEUROSCI.1380-10.2010
41. 4 muscarinic acetylcholine receptors plays a critical role in modulating dopamine-dependent behaviors J. Neurosci. 30 2010 2396 2405 10.1523/JNEUROSCI.3843-09.2010
42. D. Jerusalinsky, E. Kornisiuk, P. Alfaro, J. Quillfeldt, A. Ferreira, V.E. Rial, R. Duran, and C. Cerveñansky Muscarinic toxins: novel pharmacological tools for the muscarinic cholinergic system Toxicon 38 2000 747 761 10.1016/S0041-0101(99)00196-8
43. E. Karlsson, M. Jolkkonen, E. Mulugeta, P. Onali, and A. Adem Snake toxins with high selectivity for subtypes of muscarinic acetylcholine receptors Biochimie 82 2000 793 806 10.1016/S0300-9084(00)01176-7
44. Y. Kawaguchi, C.J. Wilson, S.J. Augood, and P.C. Emson Striatal interneurons: chemical, physiological and morphological characterization Trends Neurosci. 18 1995 527 535 10.1016/0166-2236(95)98374-8
45. A.V. Kravitz, B.S. Freeze, P.R. Parker, K. Kay, M.T. Thwin, K. Deisseroth, and A.C. Kreitzer Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry Nature 466 2010 622 626 10.1038/nature09159
46. L. Liang, M.R. DeLong, and S.M. Papa Inversion of dopamine responses in striatal medium spiny neurons and involuntary movements J. Neurosci. 28 2008 7537 7547 10.1523/JNEUROSCI.1176-08.2008
47. V.G. López-Huerta, L. Carrillo-Reid, E. Galarraga, D. Tapia, T. Fiordelisio, R. Drucker-Colin, and J. Bargas The balance of striatal feedback transmission is disrupted in a model of parkinsonism J. Neurosci. 33 2013 4964 4975 10.1523/JNEUROSCI.4721-12.2013
48. N.M. Nathanson A multiplicity of muscarinic mechanisms: enough signaling pathways to take your breath away Proc. Natl. Acad. Sci. 97 2000 6245 6247 10.1073/pnas.97.12.6245
49. E.S. Nisenbaum, C.J. Wilson, R.C. Foehring, and D.J. Surmeier Isolation and characterization of a persistent potassium current in neostriatal neurons J. Neurophysiol. 76 1996 1180 1194
50. J.A. Obeso, M.C. Rodríguez-Oroz, M. Rodríguez, J.L. Lanciego, J. Artieda, N. Gonzalo, and C.W. Olanow Pathophysiology of the basal ganglia in Parkinson's disease Trends Neurosci. 23 2000 8 19 10.1016/S1471-1931(00)00028-8
51. 1-like receptor signalling in rat nucleus accumbens Eur. J. Pharmacol. 448 2002 105 111 10.1016/S0014-2999(02)01910-6
52. P. Pakhotin, and E. Bracci Cholinergic interneurons control the excitatory input to the striatum J. Neurosci. 27 2007 391 400 10.1523/JNEUROSCI.3709-06.2007
53. K.E. Pemberton, and S.V.P. Jones Enhancement of an L-type calcium current in AtT-20 cells; a novel effect of m4 muscarinic receptor Pflug. Arch. 429 1995 699 707
54. 1 modulation of N and L types of calcium channels is mediated by PKC in neostriatal neurons Neuroscience 155 2008 1079 1097 10.1016/j.neuroscience.2008.06.047
55. 1 receptors through phosphoinositide hydrolysis in neostriatal neurons Neuroscience 165 2010 293 299 10.1016/j.neuroscience.2009.10.056
56. 2+ channels in the repetitive firing of striatal projection neurons Neuroreport 14 2003 1253 1256
57. 2+ channels J. Neurophysiol. 93 2005 2507 2519 10.1152/jn.00853.2004
58. V. Plata, M. Duhne, J. Pérez-Ortega, R. Hernández-Martinez, P. Rueda-Orozco, E. Galarraga, R. Drucker-Colín, and J. Bargas Global actions of nicotine on the striatal microcircuit Front. Syst. Neurosci. 7 78 2013 10.3389/fnsys.2013.00078
59. A. Pisani, G. Bernardi, J. Ding, and D.J. Surmeier Re-emergence of striatal cholinergic interneurons in movement disorders Trends Neurosci. 30 2007 545 553 10.1016/j.tins.2007.07.008
60. L. Prensa, and A. Parent The nigrostriatal pathway in the rat: a single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments J. Neurosci. 21 2001 7247 7260
61. 2+ current modulation in neostriatal neurons Neuroscience 164 2009 345 350 10.1016/j.neuroscience.2009.08.030
62. 2 depletion J. Neurophysiol. 105 2011 2260 2274 10.1152/jn.00516.2010
63. S.L. Purkerson, and L.T. Potter Use of antimuscarinic toxins to facilitate studies of striatal muscarinic receptors J. Pharmacol. Exp. Ther. 284 1998 707 713
64. 2 modulation in developing neostriatal neurons J. Neurophysiol. 94 2005 3771 3787 10.1152/jn.00455.2005
65. 4 muscarinic receptor protein on direct than indirect striatal projection neurons Brain Res. 894 2001 12 20 10.1016/S0006-8993(00)03170-X
66. W. Shen, S.E. Hamilton, N.M. Nathanson, and D.J. Surmeier Cholinergic suppression of KCNQ channel currents enhances excitability of striatal medium spiny neurons J. Neurosci. 25 2005 7449 7458 10.1523/JNEUROSCI.1381-05.2005
67. W. Shen, X. Tian, M. Day, S. Ulrich, T. Tkatch, N.M. Nathanson, and D.J. Surmeier Cholinergic modulation of Kir2 channels selectively elevates dendritic excitability in striatopallidal neurons Nat. Neurosci. 10 2007 1458 1466 10.1038/nn1972
68. W. Shultz Multiple dopamine functions at different time courses Annu. Rev. Neurosci. 30 2007 259 288 10.1146/annurev.neuro.28.061604.135722
69. R.J. Sizemore, J.N. Reynolds, and D.E. Oorschot Number and type of synapses on the distal dendrite of a rat striatal cholinergic interneuron: a quantitative, ultrastructural study J. Anat. 217 2010 223 235 10.1111/j.1469-7580.2010.01264.x
70. Y. Smith, M.D. Bevan, E. Shink, and J.P. Bolam Microcircuitry of the direct and indirect pathways of the basal ganglia Neuroscience 86 1998 353 387 10.1016/S0306-4522(98)00004-9
71. 2+ current J. Neurophysiol. 71 1994 1272 1280
72. 1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons Neuron 14 1995 385 397 10.1016/0896-6273(95)90294-5
73. D.J. Surmeier, L. Carrillo-Reid, and J. Bargas Dopaminergic modulation of striatal neurons, circuits, and assemblies Neuroscience 198 2011 3 18 10.1016/j.neuroscience.2011.08.051
74. K. Takakusaki Neurophysiology of gait: from the spinal cord to the frontal lobe Mov. Disord. 28 2013 1483 1491 10.1002/mds.25669
75. v2 calcium channels Pharmacol. Rev. 58 2006 837 862 10.1124/pr.58.4.11
76. S. Threlfell, and S.J. Cragg Dopamine signaling in dorsal versus ventral striatum: the dynamic role of cholinergic interneurons Front. Syst. Neurosci. 5 11 2011 10.3389/fnsys.2011.00011
77. N.X. Tritsch, and B.L. Sabatini Dopaminergic modulation of synaptic transmission in cortex and striatum Neuron 76 2012 33 50 10.1016/j.neuron.2012.09.023
78. + currents in neostriatal neurons Neuroscience 95 2000 745 752 10.1016/S0306-4522(99)00493-5
79. 2+ currents in neostriatal neurons Neuroscience 109 2002 555 567 10.1016/S0306-4522(01)00503-6
80. V2.2 channels is delimited to a specific region of the membrane potential in rat SCG neurons Acta. Biochim. Biophys. Sin. 44 2012 544 549 10.1093/abbs/gms025
81. B.J. Vizcarra-Chacón, M.A. Arias-García, M.B. Pérez-Ramirez, E. Flores-Barrera, D. Tapia, R. Drucker-Colin, J. Bargas, and E. Galarraga Contribution of different classes of glutamate receptors in the corticostriatal polysynaptic responses from striatal direct and indirect projection neurons BMC Neurosci. 14 60 2013 10.1186/1471-2202-14-60
82. Z. Yan, J. Flores-Hernández, and D.J. Surmeier Coordinated expression of muscarinic receptor messenger RNAs in striatal medium spiny neurons Neuroscience 103 2001 1017 1024 10.1016/S0306-4522(01)00039-2
83. 2+ currents in rat neostriatal cholinergic interneurons through a fast, membrane delimited, G-protein pathway J. Neurosci. 16 1996 2592 2604
84. F.M. Zhou, C.J. Wilson, and J.A. Dani Cholinergic interneuron characteristics and nicotinic properties in the striatum J. Neurobiol. Rev. 53 2002 590 605 10.1002/neu.10150