Three-photon microscopy shows that somatic release can be a quantitatively significant component of serotonergic neurotransmission in the mammalian brain

Journal of Neuroscience Research

Volumn 86, Issue 15, 2008, Pages 3469-3480

  Kaushalya, S K ^a   Desai, R ^a   Arumugam, S ^a   Ghosh, H ^a   Balaji, J ^b   Maiti, Sudipta ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Extra synaptic neurotransmission; Neurotransmitter imaging; Serotonin; Somatic exocytosis

Indexed keywords

CHLORAMPHETAMINE; POTASSIUM ION; SEROTONIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; AUTOFLUORESCENCE; BRAIN NERVE CELL; BRAIN SLICE; CONTROLLED STUDY; DEPOLARIZATION; DORSAL RAPHE NUCLEUS; FEMALE; IMMUNOHISTOCHEMISTRY; KINETICS; MAMMAL; MICROSCOPY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; SEROTONINERGIC TRANSMISSION; SYNAPSE VESICLE; THREE PHOTON MICROSCOPY;

ANIMALS; BRAIN; CELLS, CULTURED; FEMALE; IMMUNOHISTOCHEMISTRY; MICROSCOPY; MICROSCOPY, FLUORESCENCE; NEURONS; ORGAN CULTURE TECHNIQUES; RATS; RATS, WISTAR; SEROTONIN; SYNAPTIC TRANSMISSION; VACUOLES;

EID: 57049184561     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21794     Document Type: Article

References (50)

1. Adell A, Celada P, Abellan MT, Artigas F. 2002. Origin and functional role of the extracellular serotonin in the midbrain raphe nuclei. Brain Res Brain Res Rev 39:154-180.
2. Agnati LF, Zoli M, Stromberg I, Fuxe K. 1995. Intercellular communication in the brain: wiring vs. volume transmission. Neuroscience 69:711-726.
3. Azmitia EC. 1999. Serotonin neurons, neuroplasticity, and homeostasis of neural tissue. Neuropsychopharmacology 21(Suppl 2):33S-45S.
4. Balaji J, Desai R, Kaushalya SK, Eaton MJ, Maiti S. 2005. Quantitative measurement of serotonin synthesis and sequestration in individual live neuronal cells. J Neurochem 95:1217-1226.
5. Barker LA, Dowdall MJ, Whittaker VP. 1972. Choline metabolism in the cerebral cortex of guinea pigs. Stable-bound acetylcholine. Biochem J 130:1063-1075.
6. Betz WJ, Bewick GS. 1992. Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255:200-203.
7. Betz WJ, Mao F, Bewick GS. 1992. Activity-dependent fluorescent staining and destaining of living vertebrate motor nerve terminals. J Neurosci 12:363-375.
8. Brumback AC, Lieber JL, Angleson JK, Betz WJ. 2004. Using FM1-43 to study neuropeptide granule dynamics and exocytosis. Methods 33:287-294.
9. Bruns D, Jahn R. 1995. Real-time measurement of transmitter release from single synaptic vesicles. Nature 377:62-65.
10. Bruns D, Riedel D, Klingauf J, Jahn R. 2000. Quantal release of serotonin. Neuron 28:205-220.
11. Bunin MA, Wightman RM. 1998. Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission. J Neurosci 18:4854-4860.
12. Bunin MA, Wightman RM. 1999. Paracrine neurotransmission in the CNS: involvement of 5-HT. Trends Neurosci 22:377-382.
13. Chen G, Gavin PF, Luo G, Ewing AG. 1995. Observation and quantitation of exocytosis from the cell body of a fully developed neuron in Planorbis corneus. J Neurosci 15:7747-7755.
14. Cheramy A, Leviel V, Glowinski J. 1981. Dendritic release of dopamine in the substantia nigra. Nature 289:537-542.
15. Cooper JR, Bloom FE, Roth RH. 1996. The biochemical basis of neuropharmacology. New York: Oxford University Press.
16. Crespi F, Martin KF, Marsden CA. 1988. Measurement of extracellular basal levels of serotonin in vivo using na.on-coated carbon fibre electrodes combined with differential pulse voltammetry. Neuroscience 27:885-896.
17. Csaba G, Kovacs P. 2006. Perinuclear localization of biogenic amines (serotonin and histamine) in rat immune cells. Cell Biol Int 30:861-865.
18. Darzynkiewicz Z, Staiano-Coico L, Melamed MR. 1981. Increased mitochondrial uptake of rhodamine 123 during lymphocyte stimulation. Proc Natl Acad Sci U S A 78:2383-2387.
19. de Kock CP, Cornelisse LN, Burnashev N, Lodder JC, Timmerman AJ, Couey JJ, Mansvelder HD, Brussaard AB. 2006. NMDA receptors trigger neurosecretion of 5-HT within dorsal raphe nucleus of the rat in the absence of action potential firing. J Physiol 577:891-905.
20. Garris PA, Ciolkowski EL, Pastore P, Wightman RM. 1994. Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain. J Neurosci 14:6084-6093.
21. Gostkowski ML, Allen R, Plenert ML, Okerberg E, Gordon MJ, Shear JB. 2004. Multiphoton-excited serotonin photochemistry. Biophys J 86:3223-3229.
22. Henderson LP. 1983. The role of 5-hydroxytryptamine as a transmitter between identified leech neurones in culture. J Physiol 339:309-324.
23. 2+-dependent exocytosis in the somata of dorsal root ganglion neurons. Neuron 17:135-145.
24. Jaffe EH, Marty A, Schulte A, Chow RH. 1998. Extrasynaptic vesicular transmitter release from the somata of substantia nigra neurons in rat midbrain slices. J Neurosci 18:3548-3553.
25. Johnson LV, Walsh ML, Chen LB. 1980. Localization of mitochondria in living cells with rhodamine 123. Proc Natl Acad Sci U S A 77:990-994.
26. Kandel ER, Schwartz JH, Jessell TM. 2000. Principles of neural science. New York: McGraw-Hill.
27. Kaushalya SK, Maiti S. 2007. Quantitative imaging of serotonin autofluorescence with multiphoton microscopy. In: Chattopadhyay A, editor. Serotonin receptors in neurobiology. New York: CRC Press. p 1-18.
28. Kaushalya SK, Nag S, Ghosh H, Arumugam S, Maiti S. 2008. A high-resolution large area serotonin map of a live rat brain section Neuroreport 19:717-721.
29. Kia HK, Brisorgueil MJ, Hamon M, Calas A, Vergé D. 1996. Ultrastructural localization of 5-hydroxytryptamine 1A receptors in the rat brain. J Neurosci Res 46:697-708.
30. Maiti S, Shear JB, Williams R. M., Zipfel WR, Webb WW. 1997. Measuring serotonin distribution in live cells with three-photon excitation. Science 275:530-532.
31. Miao H, Rubakhin SS, Sweedler JV. 2003. Analysis of serotonin release from single neuron soma using capillary electrophoresis and laser-induced fluorescence with a pulsed deep-UV NeCu laser. Anal Bioanal Chem 377:1007-1013.
32. Nag S, Balaji J, Madhu PK, Maiti S. 2008. Intermolecular association provides specific optical and NMR signatures for serotonin at intravesicular concentrations. Biophys J 94:4145-4153.
33. Nicholls JG, Martin AR, Wallace BG, Fuchs PA. 2001. From neuron to brain. Sunderland, MA: Sinauer Associates, Inc.
34. Puopolo M, Hochstetler SE, Gustincich S, Wightman RM, Raviola E. 2001. Extrasynaptic release of dopamine in a retinal neuron: activity dependence and transmitter modulation. Neuron 30:211-225.
35. Rajaofetra N, Kachidian P, Marlier L, Poulat P, Konig N, Geffard M, Privat A. 1991. Electronmicroscopic detection of the axonal coexistence of serotonin and substance P in B1-B2 raphe cells transplanted into the transected spinal cord of adult rats. Brain Res 542:159-162.
36. Ryan TA, Smith SJ. 1995. Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14:983-989.
37. Schneggenburger R, Meyer AC, Neher E. 1999. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23:399-409.
38. Stevens CF, Tsujimoto T. 1995. Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc Natl Acad Sci U S A 92:846-849.
39. Stout AL, Axelrod D. 1989. Evanescent field excitation of fluorescence by epi-illumination microscopy. Appl Opt 28:5237-5242.
40. Trueta C, Mendez B, De-Miguel FF. 2003. Somatic exocytosis of serotonin mediated by L-type calcium channels in cultured leech neurones. J Physiol 547:405-416.
41. Van Bockstaele EJ, Pickel VM. 1993. Ultrastructure of serotonin-immunoreactive terminals in the core and shell of the rat nucleus accumbens: cellular substrates for interactions with catecholamine afferents. J Comp Neurol 334:603-617.
42. Viscio DB, Prestegard JH. 1981. NMR studies of 5-hydroxytryptamine transport through large unilamellar vesicle membranes. Proc Natl Acad Sci U S A 78:1638-1642.
43. Vishwasrao HD, Heikal AA, Kasischke KA, Webb WW. 2005. Conformational dependence of intracellular NADH on metabolic state revealed by associated fluorescence anisotropy. J Biol Chem 280: 25119-25126.
44. Wang W, Pizzonia JH, Richerson GB. 1998. Chemosensitivity of rat medullary raphe neurones in primary tissue culture. J Physiol 511:433-450.
45. White LA, Eaton MJ, Castro MC, Klose KJ, Globus MY, Shaw G, Whittemore SR. 1994. Distinct regulatory pathways control neurofilament expression and neurotransmitter synthesis in immortalized serotonergic neurons. J Neurosci 14:6744-6753.
46. Williams RM, Shear JB, Zipfel WR, Maiti S, Webb WW. 1999. Mucosal mast cell secretion processes imaged using three-photon microscopy of 5-hydroxytryptamine autofluorescence. Biophys J 76:1835-1846.
47. Zaidi ZF, Matthews MR. 1997. Exocytotic release from neuronal cell bodies, dendrites and nerve terminals in sympathetic ganglia of the rat, and its differential regulation. Neuroscience 80:861-891.
48. Zaidi ZF, Matthews MR. 1999. Stimulant-induced exocytosis from neuronal somata, dendrites, and newly formed synaptic nerve terminals in chronically decentralized sympathetic ganglia of the rat. J Comp Neurol 415:121-143.
49. Zoli M, Agnati LF. 1996. Wiring and volume transmission in the central nervous system: the concept of closed and open synapses. Prog Neurobiol 49:363-380.
50. Zoli M, Jansson A, Sykova E, Agnati LF, Fuxe K. 1999. Volume transmission in the CNS and its relevance for neuropsychopharmacology. Trends Pharmacol Sci 20:142-150.