Neurotransmitter phenotype plasticity: An unexpected mechanism in the toolbox of network activity homeostasis

Developmental Neurobiology

Volumn 72, Issue 1, 2012, Pages 22-32

  Demarque, Michaël ^a,b   Spitzer, Nicholas C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

Author keywords

Homeostasis; Neuronal activity; Neurotransmitter phenotype; Plasticity; Transmitter coexpression; Transmitter specification

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 4 AMINOBUTYRIC ACID; ACETYLCHOLINE; GLYCINE; MESSENGER RNA; NEUROTRANSMITTER; SULPIRIDE;

ANIMAL EXPERIMENT; BRAIN; CONTROLLED STUDY; EMBRYO; HIPPOCAMPUS; LIGHT ADAPTATION; MAMMAL; NERVE CELL; NERVE CELL PLASTICITY; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; XENOPUS;

ANIMALS; BRAIN; HOMEOSTASIS; NERVE NET; NEURONAL PLASTICITY; NEURONS; PHENOTYPE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 83455225211     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20909     Document Type: Review

References (69)

1. Abrajano JJ, Qureshi IA, Gokhan S, Zheng D, Bergman A, Mehler MF. 2009. REST and CoREST modulate neuronal subtype specification, maturation and maintenance. PLoS One 4: e7936.
2. Airan RD, Hu ES, Vijaykumar R, Roy M, Meltzer LA, Deisseroth K. 2007. Integration of light-controlled neuronal firing and fast circuit imaging. Curr Opin Neurobiol 17: 587-592.
3. Alenina N, Bashammakh S, Bader M. 2006. Specification and differentiation of serotonergic neurons. Stem Cell Rev 2: 5-10.
4. Allene C, Cattani A, Ackman JB, Bonifazi P, Aniksztejn L, Ben-Ari Y, Cossart R. 2008. Sequential generation of two distinct synapse-driven network patterns in developing neocortex. J Neurosci 28: 12851-12863.
5. Amilhon B, Lepicard E, Renoir T, Mongeau R, Popa D, Poirel O, Miot S, et al. 2010. VGLUT3 (vesicular glutamate transporter type 3) contribution to the regulation of serotonergic transmission and anxiety. J Neurosci 30: 2198-2210.
6. Ang SL. 2006. Transcriptional control of midbrain dopaminergic neuron development. Development 133: 3499-3506.
7. Arenkiel BR, Peca J, Davison IG, Feliciano C, Deisseroth K, Augustine GJ, Ehlers MD, et al. 2007. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54: 205-218.
8. Ben-Ari Y, Spitzer NC. 2010. Phenotypic checkpoints regulate neuronal development. Trends Neurosci 33: 485-492.
9. Berube-Carriere N, Riad M, Dal BG, Levesque D, Trudeau LE, Descarries L. 2009. The dual dopamine-glutamate phenotype of growing mesencephalic neurons regresses in mature rat brain. J Comp Neurol 517: 873-891.
10. Blankenship AG, Feller MB. 2010. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11: 18-29.
11. Borodinsky LN, Root CM, Cronin JA, Sann SB, Gu X, Spitzer NC. 2004. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429: 523-530.
12. Borodinsky LN, Spitzer NC. 2007. Activity-dependent neurotransmitter-receptor matching at the neuromuscular junction. Proc Natl Acad Sci USA 104: 335-340.
13. Boulland JL, Qureshi T, Seal RP, Rafiki A, Gundersen V, Bergersen LH, Fremeau RTJr, et al. 2004. Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J Comp Neurol 480: 264-280.
14. Brosenitsch TA, Katz DM. 2001. Physiological patterns of electrical stimulation can induce neuronal gene expression by activating N-type calcium channels. J Neurosci 21: 2571-2579.
15. Burrone J, O'Byrne M, Murthy VN. 2002. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 420: 414-418.
16. Cheng L, Arata A, Mizuguchi R, Qian Y, Karunaratne A, Gray PA, Arata S, et al. 2004. Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat Neurosci 7: 510-517.
17. Cheng L, Chen CL, Luo P, Tan M, Qiu M, Johnson R, Ma Q. 2003. Lmx1b. Pet-1, and Nkx22 coordinately specify serotonergic neurotransmitter phenotype J Neurosci 23: 9961-9967.
18. Cheng L, Samad OA, Xu Y, Mizuguchi R, Luo P, Shirasawa S, Goulding M, et al. 2005. Lbx1 and Tlx3 are opposing switches in determining GABAergic versus glutamatergic transmitter phenotypes. Nat Neurosci 8: 1510-1515.
19. Crepel V, Aronov D, Jorquera I, Represa A, Ben-Ari Y, Cossart R. 2007. A parturition-associated nonsynaptic coherent activity pattern in the developing hippocampus. Neuron 54: 105-120.
20. Demarque M, Represa A, Becq H, Khalilov I, Ben-Ari Y, Aniksztejn L. 2002. Paracrine intercellular communication by a Ca2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron 36: 1051-1061.
21. Demarque M, Spitzer NC. 2010. Activity-dependent expression of Lmx1b regulates specification of serotonergic neurons modulating swimming behavior. Neuron 67: 321-334.
22. Ding YQ, Marklund U, Yuan W, Yin J, Wegman L, Ericson J, Deneris E, et al. 2003. Lmx1b is essential for the development of serotonergic neurons. Nat Neurosci 6: 933-938.
23. Dulcis D, Spitzer NC. 2008. Illumination controls differentiation of dopamine neurons regulating behaviour. Nature 456: 195-201.
24. Furshpan EJ, MacLeish PR, O'Lague PH, Potter DD. 1976. Chemical transmission between rat sympathetic neurons and cardiac myocytes developing in microcultures: Evidence for cholinergic, adrenergic, and dual-function neurons. Proc Natl Acad Sci USA 73: 4225-4229.
25. Gillespie DC, Kim G, Kandler K. 2005. Inhibitory synapses in the developing auditory system are glutamatergic. Nat Neurosci 8: 332-338.
26. Gomez-Lira G, Lamas M, Romo-Parra H, Gutierrez R. 2005. Programmed and induced phenotype of the hippocampal granule cells. J Neurosci 25: 6939-6946.
27. Goulding M. 2009. Circuits controlling vertebrate locomotion: Moving in a new direction. Nat Rev Neurosci 10: 507-518.
28. Gradinaru V, Thompson KR, Zhang F, Mogri M, Kay K, Schneider MB, Deisseroth K. 2007. Targeting and readout strategies for fast optical neural control in vitro and in vivo. J Neurosci 27: 14231-14238.
29. Gras C, Herzog E, Bellenchi GC, Bernard V, Ravassard P, Pohl M, Gasnier B, et al. 2002. A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 22: 5442-5451.
30. Grashow R, Brookings T, Marder E. 2009. Reliable neuromodulation from circuits with variable underlying structure. Proc Natl Acad Sci USA 106: 11742-11746.
31. Grubb MS, Burrone J. 2010. Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 465: 1070-1074.
32. Gutierrez R. 2002. Activity-dependent expression of simultaneous glutamatergic and GABAergic neurotransmission from the mossy fibers in vitro. J Neurophysiol 87: 2562-2570.
33. Gutierrez R, Heinemann U. 2006. Co-existence of GABA and Glu in the hippocampal granule cells: Implications for epilepsy. Curr Top Med Chem 6: 975-978.
34. Gutierrez R, Romo-Parra H, Maqueda J, Vivar C, Ramirez M, Morales MA, Lamas M. 2003. Plasticity of the GABAergic phenotype of the "glutamatergic" granule cells of the rat dentate gyrus. J Neurosci 23: 5594-5598.
35. Hanson MG, Landmesser LT. 2003. Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. J Neurosci 23: 587-600.
36. Hnasko TS, Chuhma N, Zhang H, Goh GY, Sulzer D, Palmiter RD, Rayport S, et al. 2010. Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron 65: 643-656.
37. Hokfelt T, Elfvin LG, Elde R, Schultzberg M, Goldstein M, Luft R. 1977. Occurrence of somatostatin-like immunoreactivity in some peripheral sympathetic noradrenergic neurons. Proc Natl Acad Sci USA 74: 3587-3591.
38. Hokfelt T, Johansson O, Ljungdahl A, Lundberg JM, Schultzberg M. 1980. Peptidergic neurones. Nature 284: 515-521.
39. Janovjak H, Szobota S, Wyart C, Trauner D, Isacoff EY. 2010. A light-gated, potassium-selective glutamate receptor for the optical inhibition of neuronal firing. Nat Neurosci 13: 1027-1032.
40. Jonas P, Bischofberger J, Hler J. 1998. Corelease of two fast neurotransmitters at a central synapse. Science 281: 419-424.
41. Kastanenka KV, Landmesser LT. 2010. In vivo activation of channelrhodopsin-2 reveals that normal patterns of spontaneous activity are required for motoneuron guidance and maintenance of guidance molecules. J Neurosci 30: 10575-10585.
42. Kim DS, Kim JE, Kwak SE, Kim DW, Choi SY, Kwon OS, Kang TC. 2007. Seizure activity selectively reduces 5-HT1A receptor immunoreactivity in CA1 interneurons in the hippocampus of seizure-prone gerbils. Brain Res 1154: 181-193.
43. Landis SC. 1990. Target regulation of neurotransmitter phenotype. Trends Neurosci 13: 344-350.
44. Li X, Gutierrez DV, Hanson MG, Han J, Mark MD, Chiel H, Hegemann P, et al. 2005. Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc Natl Acad Sci USA 102: 17816-17821.
45. LoTurco J, Manent JB, Sidiqi F. 2009. New and improved tools for in utero electroporation studies of developing cerebral cortex. Cereb Cortex 19( Suppl 1): i120-i125.
46. Mancuso JJ, Kim J, Lee S, Tsuda S, Chow NB, Augustine GJ. 2011. Optogenetic probing of functional brain circuitry. Exp Physiol 96: 26-33.
47. Manent JB, Demarque M, Jorquera I, Pellegrino C, Ben-Ari Y, Aniksztejn L, Represa A. 2005. A noncanonical release of GABA and glutamate modulates neuronal migration. J Neurosci 25: 4755-4765.
48. Marder E. Quantification of behavior sackler colloquium: Variability, compensation, and modulation in neurons and circuits. Proc Natl Acad Sci USA, in press.
49. Marek KW, Kurtz LM, Spitzer NC. 2010. cJun integrates calcium activity and tlx3 expression to regulate neurotransmitter specification. Nat Neurosci 13: 944-950.
50. McLaughlin T, Torborg CL, Feller MB, O'Leary DD. 2003. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 40: 1147-1160.
51. Milner LD, Landmesser LT. 1999. Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. J Neurosci 19: 3007-3022.
52. Nabekura J, Katsurabayashi S, Kakazu Y, Shibata S, Matsubara A, Jinno S, Mizoguchi Y, et al. 2004. Developmental switch from GABA to glycine release in single central synaptic terminals. Nat Neurosci 7: 17-23.
53. Nishimaru H, Restrepo CE, Ryge J, Yanagawa Y, Kiehn O. 2005. Mammalian motor neurons corelease glutamate and acetylcholine at central synapses. Proc Natl Acad Sci USA 102: 5245-5249.
54. Noh J, Seal RP, Garver JA, Edwards RH, Kandler K. 2010. Glutamate co-release at GABA/glycinergic synapses is crucial for the refinement of an inhibitory map. Nat Neurosci 13: 232-238.
55. Pozo K, Goda Y. 2010. Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66: 337-351.
56. Root CM, Velazquez-Ulloa NA, Monsalve GC, Minakova E, Spitzer NC. 2008. Embryonically expressed GABA and glutamate drive electrical activity regulating neurotransmitter specification. J Neurosci 28: 4777-4784.
57. Safiulina VF, Caiati MD, Sivakumaran S, Bisson G, Migliore M, Cherubini E. 2010. Control of GABA release at mossy fiber-CA3 connections in the developing hippocampus. Front Synaptic Neurosci 2: 1.
58. Safiulina VF, Fattorini G, Conti F, Cherubini E. 2006. GABAergic signaling at mossy fiber synapses in neonatal rat hippocampus. J Neurosci 26: 597-608.
59. Scain AL, Le CH, Allain AE, Muller E, Rigo JM, Meyrand P, Branchereau P, et al. 2010. Glycine release from radial cells modulates the spontaneous activity and its propagation during early spinal cord development. J Neurosci 30: 390-403.
60. Scott MM, Deneris ES. 2005. Making and breaking serotonin neurons and autism. Int J Dev Neurosci 23: 277-285.
61. Scott MM, Wylie CJ, Lerch JK, Murphy R, Lobur K, Herlitze S, Jiang W, et al. 2005. A genetic approach to access serotonin neurons for in vivo and in vitro studies. Proc Natl Acad Sci USA 102: 16472-16477.
62. Seal RP, Edwards RH. 2006. Functional implications of neurotransmitter co-release: Glutamate and GABA share the load. Curr Opin Pharmacol 6: 114-119.
63. Soussi R, Zhang N, Tahtakran S, Houser CR, Esclapez M. 2010. Heterogeneity of the supramammillary-hippocampal pathways: Evidence for a unique GABAergic neurotransmitter phenotype and regional differences. Eur J Neurosci 32: 771-785.
64. Trudeau LE, Gutierrez R. 2007. On cotransmission & neurotransmitter phenotype plasticity. Mol Interv 7: 138-146.
65. Turrigiano GG, Nelson SB. 2000. Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol 10: 358-364.
66. Turrigiano GG, Nelson SB. 2004. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5: 97-107.
67. Velazquez-Ulloa NA, Spitzer NC, Dulcis D. 2011. Contexts for dopamine specification by calcium spike activity in the CNS. J Neurosci 31: 78-88.
68. Walicke PA, Patterson PH. 1981. On the role of Ca2+ in the transmitter choice made by cultured sympathetic neurons. J Neurosci 1: 343-350.
69. Zhao ZQ, Scott M, Chiechio S, Wang JS, Renner KJ, Gereau RW, Johnson RL, et al. 2006. Lmx1b is required for maintenance of central serotonergic neurons and mice lacking central serotonergic system exhibit normal locomotor activity. J Neurosci 26:12781-12788.