Cotransmission of acetylcholine and GABA

Neuropharmacology

Volumn 100, Issue , 2016, Pages 40-46

  Granger, Adam J ^a   Mulder, Nicole ^a   Saunders, Arpiar ^a   Sabatini, Bernardo L ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Acetylcholine; Cotransmission; GABA; Neurotransmitter corelease

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; ACETYLCHOLINE; CHOLINERGIC RECEPTOR; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; GLYCINE RECEPTOR; SCAFFOLD PROTEIN;

ACETYLCHOLINE RELEASE; ANIMAL TISSUE; BRAIN CORTEX; CHOLINERGIC NERVE CELL; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; ENZYME LOCALIZATION; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; REVIEW; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN; HUMAN; METABOLISM;

ACETYLCHOLINE; ANIMALS; BRAIN; CHOLINERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; HUMANS; MICE; OPTOGENETICS; SYNAPTIC TRANSMISSION;

EID: 84942364579     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.07.031     Document Type: Review

References (78)

1. S. Arroyo, C. Bennett, and D. Aziz Prolonged disynaptic inhibition in the cortex mediated by slow, non-α7 nicotinic excitation of a specific subset of cortical interneurons J. Neurosci. 32 2012 3859 3864
2. S. Arroyo, C. Bennett, and S. Hestrin Nicotinic modulation of cortical circuits Front. Neural Circuits 8 2014 30
3. C. Beaulieu, and P. Somogyi Enrichment of cholinergic synaptic terminals on GABAergic neurons and coexistence of immunoreactive GABA and choline acetyltransferase in the same synaptic terminals in the striate cortex of the cat J. Comp. Neurol. 304 1991 666 680
4. C. Bennett, S. Arroyo, D. Berns, and S. Hestrin Mechanisms generating dual-component nicotinic EPSCs in cortical interneurons J. Neurosci. 32 2012 17287 17296
5. N. Brecha, D. Johnson, L. Peichl, and H. Wässle Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity Proc. Natl. Acad. Sci. U. S. A. 85 1988 6187 6191
6. P. Calabresi, D. Centonze, P. Gubellini, A. Pisani, and G. Bernardi Acetylcholine-mediated modulation of striatal function Trends Neurosci. 23 2000 120 126
7. J.H. Caldwell, N.W. Daw, and H.J. Wyatt Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields J. Physiol. 276 1978 277 298
8. B. Cauli, X. Zhou, L. Tricoire, X. Toussay, and J.F. Staiger Revisiting enigmatic cortical calretinin-expressing interneurons Front. Neuroanat. 8 2014 52
9. J.R. Chalifoux, and A.G. Carter GABAB receptor modulation of synaptic function Curr. Opin. Neurobiol. 21 2011 339 344
10. S. Consonni, S. Leone, A. Becchetti, and A. Amadeo Developmental and neurochemical features of cholinergic neurons in the murine cerebral cortex BMC Neurosci. 10 2009 18
11. C.B. Duarte, P.F. Santos, and A.P. Carvalho Corelease of two functionally opposite neurotransmitters by retinal amacrine cells: experimental evidence and functional significance J. Neurosci. Res. 58 1999 475 479
12. E. Eggermann, Y. Kremer, S. Crochet, and C.C.H. Petersen Cholinergic signals in mouse barrel cortex during active Whisker sensing Cell Rep. 9 2014 1654 1660
13. J. Von Engelhardt, M. Eliava, A.H. Meyer, A. Rozov, and H. Monyer Functional characterization of intrinsic cholinergic interneurons in the cortex J. Neurosci. 27 2007 5633 5642
14. K.L. Engisch, and G.D. Fischbach The development of ACH- and GABA-activated currents in normal and target-deprived embryonic chick ciliary ganglia Dev. Biol. 139 1990 417 426
15. K.L. Engisch, and G.D. Fischbach The development of ACh- and GABA-activated currents in embryonic chick ciliary ganglion neurons in the absence of innervation in vivo J. Neurosci. 12 1992 1115 1125
16. R.S. Fisher, and M.S. Levine Transmitter cosynthesis by corticopetal basal forebrain neurons Brain Res. 491 1989 163 168
17. M. Frotscher, M. Schlander, and C. Léránth Cholinergic neurons in the hippocampus. A combined light- and electron-microscopic immunocytochemical study in the rat Cell Tissue Res. 246 1986 293 301
18. M. Frotscher, I. Vida, and R. Bender Evidence for the existence of non-GABAergic, cholinergic interneurons in the rodent hippocampus Neuroscience 96 2000 27 31 http://www.ncbi.nlm.nih.gov/pubmed/10683406
19. Y. Fu, J.M. Tucciarone, J.S. Espinosa, N. Sheng, D.P. Darcy, R.A. Nicoll, Z.J. Huang, and M.P. Stryker A cortical circuit for gain control by behavioral state Cell 156 2014 1139 1152
20. C. Gras, E. Herzog, G.C. Bellenchi, V. Bernard, P. Ravassard, M. Pohl, B. Gasnier, B. Giros, and S. El Mestikawy A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons J. Neurosci. 22 2002 5442 5451
21. I. Gritti, L. Mainville, and B.E. Jones Codistribution of GABA- with acetylcholine-synthesizing neurons in the basal forebrain of the rat J. Comp. Neurol. 329 1993 438 457
22. I. Gritti, L. Mainville, M. Mancia, and B.E. Jones GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat J. Comp. Neurol. 383 1997 163 177
23. M.E. Hasselmo, and M. Sarter Modes and models of forebrain cholinergic neuromodulation of cognition Neuropsychopharmacology 36 2011 52 73
24. P. Henny, and B.E. Jones Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glutamatergic inputs to pyramidal cells or interneurons Eur. J. Neurosci 27 2008 654 670
25. M.J. Higley, A.H. Gittis, I.A. Oldenburg, N. Balthasar, R.P. Seal, R.H. Edwards, B.B. Lowell, A.C. Kreitzer, and B.L. Sabatini Cholinergic interneurons mediate fast VGluT3-dependent glutamatergic transmission in the striatum PLoS One 6 2011 e19155
26. T.S. Hnasko, and R.H. Edwards Neurotransmitter corelease: mechanism and physiological role Annu. Rev. Physiol. 74 2012 225 243
27. L. Jiang, G.Y. López-Hernández, J. Lederman, D.A. Talmage, and L.W. Role Optogenetic studies of nicotinic contributions to cholinergic signaling in the central nervous system Rev. Neurosci. 25 2014 755 771
28. P. Jonas, J. Bischofberger, and J. Sandkühler Corelease of two fast neurotransmitters at a central synapse Science 281 1998 419 424
29. B.E. Jones Activity, modulation and role of basal forebrain cholinergic neurons innervating the cerebral cortex Prog. Brain Res. 145 2004 157 169
30. A. Kalmbach, T. Hedrick, and J. Waters Selective optogenetic stimulation of cholinergic axons in neocortex J. Neurophysiol. 107 2012 2008 2019
31. A. Kalmbach, and J. Waters Modulation of high- and low-frequency components of the cortical local field potential via nicotinic and muscarinic acetylcholine receptors in anesthetized mice J. Neurophysiol. 111 2014 258 272
32. H. Kawai, W. Zago, and D.K. Berg Nicotinic alpha 7 receptor clusters on hippocampal GABAergic neurons: regulation by synaptic activity and neurotrophins. [Online] J. Neurosci 22 2002 7903 7912 http://www.ncbi.nlm.nih.gov/pubmed/12223543 27.07.15
33. B. Kolisnyk, M.S. Guzman, S. Raulic, J. Fan, A.C. Magalhães, G. Feng, R. Gros, V.F. Prado, and M.A.M. Prado ChAT-ChR2-EYFP mice have enhanced motor endurance but show deficits in attention and several additional cognitive domains J. Neurosci. 33 2013 10427 10438
34. J.R. Köppen, S.S. Winter, S.L. Stuebing, J.L. Cheatwood, and D.G. Wallace Infusion of GAT1-saporin into the medial septum/vertical limb of the diagonal band disrupts self-movement cue processing and spares mnemonic function Brain Struct. Funct. 218 2013 1099 1114
35. T. Kosaka, M. Tauchi, and J.L. Dahl Cholinergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat Exp. Brain Res. 70 1988 605 617
36. T. Kosaka, M. Tauchi, and L. Dahl Cholinergic neurons containing GABA-Iike and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat Exp. Brain Res. 70 1988 605 617
37. S. Lee, K. Kim, and Z.J. Zhou Role of ACh-GABA cotransmission in detecting image motion and motion direction Neuron 68 2010 1159 1172
38. J.J. Letzkus, S.B.E. Wolff, E.M.M. Meyer, P. Tovote, J. Courtin, C. Herry, and A. Lu A disinhibitory microcircuit for associative fear learning in the auditory cortex Nature 480 2011 331 335
39. M. Ma, and M. Luo Optogenetic activation of basal forebrain cholinergic neurons modulates neuronal excitability and sensory responses in the main olfactory bulb J. Neurosci. 32 2012 10105 10116
40. R.H. Masland, J.W. Mills, and C. Cassidy The functions of acetylcholine in the rabbit retina Proc. R. Soc. Lond. Ser. B Biol. Sci. 223 1984 121 139
41. A.E. McEachern, J.F. Margiotta, and D.K. Berg gamma-Aminobutyric acid receptors on chick ciliary ganglion neurons in vivo and in cell culture J. Neurosci. 5 1985 2690 2695
42. S. El Mestikawy, A. Wallén-Mackenzie, G.M. Fortin, L. Descarries, and L.-E. Trudeau From glutamate co-release to vesicular synergy: vesicular glutamate transporters Nat. Rev. Neurosci. 12 2011 204 216
43. D.A. Nagode, A.-H. Tang, M.A. Karson, M. Klugmann, and B.E. Alger Optogenetic release of ACh induces rhythmic bursts of perisomatic IPSCs in hippocampus PLoS One 6 2011 e27691
44. D.M. O'Malley, and R.H. Masland Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron Proc. Natl. Acad. Sci. U. S. A. 86 1989 3414 3418
45. K.C.H. Pang, X. Jiao, S. Sinha, K.D. Beck, and R.J. Servatius Damage of GABAergic neurons in the medial septum impairs spatial working memory and extinction of active avoidance: effects on proactive interference Hippocampus 21 2011 835 846
46. L. Petreanu, T. Mao, S.M. Sternson, and K. Svoboda The subcellular organization of neocortical excitatory connections Nature 457 2009 1142 1145
47. H.-J. Pi, B. Hangya, D. Kvitsiani, J.I. Sanders, Z.J. Huang, and A. Kepecs Cortical interneurons that specialize in disinhibitory control Nature 503 2013 521 524
48. M.R. Picciotto, M.J. Higley, and Y.S. Mineur Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior Neuron 76 2012 116 129
49. L. Pinto, M.J. Goard, D. Estandian, M. Xu, A.C. Kwan, S.-H. Lee, T.C. Harrison, G. Feng, and Y. Dan Fast modulation of visual perception by basal forebrain cholinergic neurons Nat. Neurosci. 16 2013 1857 1863
50. J.J. Roland, A.L. Stewart, K.L. Janke, M.R. Gielow, J.A. Kostek, L.M. Savage, R.J. Servatius, and K.C.H. Pang Medial septum-diagonal band of Broca (MSDB) GABAergic regulation of hippocampal acetylcholine efflux is dependent on cognitive demands J. Neurosci. 34 2014 506 514
51. H. Romo-Parra, C. Vivar, J. Maqueda, M.A. Morales, and R. Gutiérrez Activity-dependent induction of multitransmitter signaling onto pyramidal cells and interneurons of hippocampal area CA3 J. Neurophysiol. 89 2003 3155 3167
52. D.H. Root, C.A. Mejias-Aponte, S. Zhang, H.-L. Wang, A.F. Hoffman, C.R. Lupica, and M. Morales Single rodent mesohabenular axons release glutamate and GABA Nat. Neurosci. 17 2014 1542 1551 10.1038/nn.3823
53. B. Rudy, G. Fishell, S. Lee, and J. Hjerling-Leffler Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons Dev. Neurobiol. 71 2011 45 61
54. P.F. Santos, A.L. Carvalho, A.P. Carvalho, and C.B. Duarte Differential acetylcholine and GABA release from cultured chick retina cells Eur. J. Neurosci. 10 1998 2723 2730
55. M. Sarter, V. Parikh, and W.M. Howe Phasic acetylcholine release and the volume transmission hypothesis: time to move on Nat. Rev. Neurosci. 10 2009 383 390
56. A. Saunders, A.J. Granger, and B.L. Sabatini Corelease of acetylcholine and GABA from cholinergic forebrain neurons Elife 4 2015
57. A. Saunders, I.A. Oldenburg, V.K. Berezovskii, C.A. Johnson, N.D. Kingery, H.L. Elliott, T. Xie, C.R. Gerfen, and B.L. Sabatini A direct GABAergic output from the basal ganglia to frontal cortex Nature 521 2015 85 89
58. S.J. Shabel, C.D. Proulx, J. Piriz, and R. Malinow GABA/glutamate co-release controls habenula output and is modified by antidepressant treatment Science 345 2014 1494 1498
59. A.N. Shrivastava, A. Triller, and W. Sieghart GABA(A) receptors: post-Synaptic co-localization and cross-talk with other receptors Front. Cell Neurosci. 5 2011 7
60. J.-J. Soghomonian, and D.L. Martin Two isoforms of glutamate decarboxylase: why? Trends Pharmacol. Sci. 19 1998 500 505
61. H. Steiner, and C.R. Gerfen Role of dynorphin and enkephalin in the regulation of striatal output pathways and behavior Exp. Brain Res. 123 1998 60 76
62. G.D. Stuber, T.S. Hnasko, J.P. Britt, R.H. Edwards, and A. Bonci Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate J. Neurosci. 30 2010 8229 8233
63. F. Tecuapetla, J.C. Patel, H. Xenias, D. English, I. Tadros, F. Shah, J. Berlin, K. Deisseroth, M.E. Rice, J.M. Tepper, and T. Koos Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens J. Neurosci. 30 2010 7105 7110
64. L.M. Teles-Grilo Ruivo, and J.R. Mellor Cholinergic modulation of hippocampal network function Front. Synaptic Neurosci. 5 2013 2
65. T. Tkatch, G. Baranauskas, and D.J. Surmeier Basal forebrain neurons adjacent to the globus pallidus co-express GABAergic and cholinergic marker mRNAs Neuroreport 9 1998 1935 1939
66. N.X. Tritsch, J.B. Ding, and B.L. Sabatini Dopaminergic neurons inhibit striatal output through non-canonical release of GABA Nature 490 2012 262 266
67. N.X. Tritsch, W.-J. Oh, C. Gu, and B.L. Sabatini Midbrain dopamine neurons sustain inhibitory transmission using plasma membrane uptake of GABA, not synthesis Elife 3 2014 e01936
68. C.T. Unal, D. Pare, and L. Zaborszky Impact of basal forebrain cholinergic inputs on basolateral amygdala neurons J. Neurosci. 35 2015 853 863
69. C.E. Vaaga, M. Borisovska, and G.L. Westbrook Dual-transmitter neurons: functional implications of co-release and co-transmission Curr. Opin. Neurobiol. 29 2014 25 32
70. D.I. Vaney, and H.M. Young GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina Brain Res. 438 1988 369 373
71. V. Varga, A. Losonczy, B.V. Zemelman, Z. Borhegyi, G. Nyiri, A. Domonkos, B. Hangya, N. Holderith, J.C. Magee, and T.F. Freund Fast synaptic subcortical control of hippocampal circuits Science 326 2009 449 453
72. T. Voigt Cholinergic amacrine cells in the rat retina J. Comp. Neurol. 248 1986 19 35
73. I.B. Witten, S.-C. Lin, M. Brodsky, R. Prakash, I. Diester, P. Anikeeva, V. Gradinaru, C. Ramakrishnan, and K. Deisseroth Cholinergic interneurons control local circuit activity and cocaine conditioning Science 330 2010 1677 1681
74. H.J. Wyatt, and N.W. Day Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina Science 191 1976 204 205
75. C. Yang, J.T. McKenna, J.C. Zant, S. Winston, R. Basheer, and R.E. Brown Cholinergic neurons excite cortically projecting Basal forebrain GABAergic neurons J. Neurosci. 34 2014 2832 2844
76. F. Yi, E. Catudio-Garrett, R. Gábriel, M. Wilhelm, F. Erdelyi, G. Szabo, K. Deisseroth, and J. Lawrence Hippocampal "cholinergic interneurons" visualized with the choline acetyltransferase promoter: anatomical distribution, intrinsic membrane properties, neurochemical characteristics, and capacity for cholinergic modulation Front. Synaptic Neurosci. 7 2015
77. W.M. Zago, K.A. Massey, and D.K. Berg Nicotinic activity stabilizes convergence of nicotinic and GABAergic synapses on filopodia of hippocampal interneurons Mol. Cell. Neurosci 31 2006 549 559
78. S. Zhao, J.T. Ting, H.E. Atallah, L. Qiu, J. Tan, B. Gloss, G.J. Augustine, K. Deisseroth, M. Luo, A.M. Graybiel, and G. Feng Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function Nat. Methods 8 2011 745 752