Abstract

The vital molecule serotonin modulates the functioning of the nervous system. The chemical characteristics of serotonin provide multiple advantages for its study in living or fixed tissue. Serotonin has the capacity to emit fluorescence directly and indirectly through chemical intermediates in response to mono- and multiphoton excitation. However, the fluorescent emissions are multifactorial and their dependence on the concentration, excitation wavelength and laser intensity still need a comprehensive study. Here we studied the fluorescence of serotonin excited multiphotonically with near-infrared light. Experiments were conducted in a custom-made multiphoton microscope coupled to a monochromator and a photomultiplier that collected the emissions. We show that the responses of serotonin to multiphoton stimulation are highly non-linear. The well-known violet emission having a 340 nm peak was accompanied by two other emissions in the visible spectrum. The best excitor wavelength to produce both emissions was 700 nm. A green emission with a ∼ 500 nm peak was similar to a previously described fluorescence in response to longer excitation wavelengths. A new blue emission with a ∼ 405 nm peak was originated from the photoconversion of serotonin to a relatively stable product. Such a reaction could be reproduced by irradiation of serotonin with high laser power for 30 minutes. The absorbance of the new compound expanded from ∼ 315 to ∼ 360 nm. Excitation of the irradiated solution monophotonically with 350 nm or biphotonically with 700 nm similarly generated the 405 nm blue emission. Our data are presented quantitatively through the design of a single geometric chart that combines the intensity of each emission in response to the serotonin concentration, excitation wavelengths and laser intensity. The autofluorescence of serotonin in addition to the formation of the two compounds emitting in the visible spectrum provides diverse possibilities for the quantitative study of the dynamics of serotonin in living tissue.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2018 (3)

E. Del-bel, F. F. De-miguel, and M. E. Rice, “Extrasynaptic neurotransmission mediated by exocytosis and diffusive release of transmitter substances,” Front. Synaptic Neurosci. 10, 13 (2018).
[Crossref]

E. Quentin, A. Belmer, and L. Maroteaux, “Somato-dendritic regulation of raphe serotonin neurons; a key to antidepressant action,” Front. Neurosci. 12, 982 (2018).
[Crossref]

B. K. Maity and S. Maiti, “Label-free imaging of neurotransmitters in live brain tissue by multi-photon ultraviolet microscopy,” Neuronal Signaling 2(4), NS20180132 (2018).
[Crossref]

2017 (1)

A. K. Das, B. K. Maity, D. Surendran, U. Tripathy, and S. Maiti, “Label-free ratiometric imaging of serotonin in live cells,” ACS Chem. Neurosci. 8(11), 2369–2373 (2017).
[Crossref]

2016 (2)

L. Shi, L. A. Sordillo, A. Rodríguez-Contreras, and R. Alfano, “Transmission in near-infrared optical windows for deep brain imaging,” J. Biophotonics 9(1-2), 38–43 (2016).
[Crossref]

L. Silvestri, I. Costantini, L. Sacconi, and F. S. Pavone, “Clearing of fixed tissue: a review from a microscopist’s perspective,” J. Biomed. Opt. 21(8), 081205 (2016).
[Crossref]

2015 (3)

Y. Aoyagi, R. Kawakami, H. Osanai, T. Hibi, and T. Nemoto, “A rapid optical clearing protocol using 2,2’-thiodiethanol for microscopic observation of fixed mouse brain,” PLoS One 21, 081205 (2015).
[Crossref]

D. O. Borroto-Escuela, L. F. Agnati, K. Bechter, A. Jansson, A. O. Tarakanov, and K. Fuxe, “The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural-glial networks,” Philos. Trans. R. Soc., B 370(1672), 20140183 (2015).
[Crossref]

F. F. De-Miguel and J. G. Nicholls, “Release of chemical transmitters from cell bodies and dendrites of nerve cells,” Philos. Trans. R. Soc., B 370(1672), 20140181 (2015).
[Crossref]

2014 (1)

R. Tomer, L. Ye, B. Hsueh, and K. Deisseroth, “Advanced clarity for rapid and high-resolution imaging of intact tissues,” Nat. Protoc. 9(7), 1682–1697 (2014).
[Crossref]

2013 (1)

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[Crossref]

2012 (1)

K. Fuxe, D. O. Borroto-Escuela, W. Romero-Fernandez, Z. Diaz-Cabiale, A. Rivera, L. Ferraro, S. Tanganelli, A. O. Tarakanov, P. Garriga, J. A. Narváez, F. Ciruela, M. Guescini, and L. F. Agnati, “Extrasynaptic neurotransmission in the modulation of brain function. focus on the striatal neuronal-glial networks,” Front. Physio. 3, 136 (2012).
[Crossref]

2011 (1)

K. Bindra, C. Singh, S. Oak, R. Sailaja, and P. Bisht, “Effect of nonlinear absorption in estimation of order of nonlinear optical process by fluorescence intensity,” Opt. Laser Technol. 43(8), 1486–1490 (2011).
[Crossref]

2008 (2)

S. K. Kaushalya, R. Desai, S. Arumugam, H. Ghosh, J. Balaji, and S. Maiti, “Three-photon microscopy shows that somatic release can be a quantitatively significant component of serotonergic neurotransmission in the mammalian brain,” J. Neurosci. Res. 86(15), 3469–3480 (2008).
[Crossref]

S. K. Kaushalya, S. Nag, J. Balaji, and S. Maiti, “Serotonin multiphoton imaging and relevant spectral data,” Proc. SPIE 6860, 68601C (2008).
[Crossref]

2007 (1)

K. Fuxe, S. Ferré, S. Genedani, R. Franco, and L. F. Agnati, “Adenosine receptor-dopamine receptor interactions in the basal ganglia and their relevance for brain function,” Physiol. Behav. 92(1-2), 210–217 (2007).
[Crossref]

2005 (2)

F. F. De-Miguel and C. Trueta, “Synaptic and extrasynaptic secretion of serotonin,” Cell. Mol. Neurobiol. 25(2), 297–312 (2005).
[Crossref]

J. Balaji, R. Desai, S. K. Kaushalya, M. J. Eaton, and S. Maiti, “Quantitative measurement of serotonin synthesis and sequestration in individual live neuronal cells,” J. Neurochem. 95(5), 1217–1226 (2005).
[Crossref]

2004 (2)

M. L. Gostkowski, R. Allen, M. L. Plenert, E. Okerberg, M. J. Gordon, and J. B. Shear, “Multiphoton-excited serotonin photochemistry,” Biophys. J. 86(5), 3223–3229 (2004).
[Crossref]

J. Balaji, R. Desai, and S. Maiti, “Live cell ultraviolet microscopy: A comparison between two- and three-photon excitation,” Microsc. Res. Tech. 63(1), 67–71 (2004).
[Crossref]

2003 (1)

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref]

2001 (1)

P. J. Campagnola, H. A. Clark, W. A. Mohler, A. Lewis, and L. M. Loew, “Second-harmonic imaging microscopy of living cells,” J. Biomed. Opt. 6(3), 277–286 (2001).
[Crossref]

2000 (3)

M. L. Gostkowski, T. E. Curey, E. Okerberg, T. J. Kang, D. A. Vanden Bout, and J. B. Shear, “Effects of molecular oxygen on multiphoton-excited photochemical analysis of hydroxyindoles,” Anal. Chem. 72(16), 3821–3825 (2000).
[Crossref]

E. A. Kravitz, “Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior,” J. Comp. Physiol. A 186(3), 221–238 (2000).
[Crossref]

D. Bruns, D. Riedel, J. Klingauf, and R. Jahn, “Quantal release of serotonin,” Neuron 28(1), 205–220 (2000).
[Crossref]

1999 (1)

R. M. Williams, J. B. Shear, W. R. Zipfel, S. Maiti, and W. W. Webb, “Mucosal mast cell secretion processes imaged using three-photon microscopy of 5-hydroxytryptamine autofluorescence,” Biophys. J. 76(4), 1835–1846 (1999).
[Crossref]

1998 (1)

M. A. Bunin and R. M. Wightman, “Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission,” J. Neurosci. 18(13), 4854–4860 (1998).
[Crossref]

1997 (3)

W. A. Weiger, “Serotonergic modulation of behaviour: a phylogenetic overview,” Biol. Rev. 72(1), 61–95 (1997).
[Crossref]

J. B. Shear, C. Xu, and W. W. Webb, “Multiphoton-excited visible emission by serotonin solutions,” Photochem. Photobiol. 65(6), 931–936 (1997).
[Crossref]

S. Maiti, J. B. Shear, R. M. Williams, W. R. Zipfel, and W. W. Webb, “Measuring serotonin distribution in live cells with three-photon excitation,” Science 275(5299), 530–532 (1997).
[Crossref]

1996 (1)

A. Chattopadhyay, R. Rukmini, and S. Mukherjee, “Photophysics of a neurotransmitter: ionization and spectroscopic properties of serotonin,” Biophys. J. 71(4), 1952–1960 (1996).
[Crossref]

1993 (1)

G. A. de Toledo, R. Fernández-Chacón, and J. M. Fernández, “Release of secretory products during transient vesicle fusion,” Nature 363(6429), 554–558 (1993).
[Crossref]

1977 (1)

T. Kishi, M. Tanaka, and J. Tanaka, “Electronic absorption and fluorescence spectra of 5-hydroxytryptamine (serotonin). protonation in the excited state,” Bull. Chem. Soc. Jpn. 50(5), 1267–1271 (1977).
[Crossref]

1968 (1)

R. F. Chen, “Fluorescence of protonated excited-state forms of 5-hydroxytryptamine (serotonin) and related indoles,” Proc. Natl. Acad. Sci. U. S. A. 60(2), 598–605 (1968).
[Crossref]

1957 (1)

D. E. Duggan, R. L. Bowman, B. B. Brodie, and S. Udenfriend, “A spectrophotofluorometric study of compounds of biological interest,” Arch. Biochem. Biophys. 68(1), 1–14 (1957).
[Crossref]

1955 (1)

S. Udenfriend, D. F. Bogdanski, and W. Herbert, “Fluorescence characteristics of 5-hydroxytryptamine (serotonin),” Science 122(3177), 972–973 (1955).
[Crossref]

Agnati, L. F.

D. O. Borroto-Escuela, L. F. Agnati, K. Bechter, A. Jansson, A. O. Tarakanov, and K. Fuxe, “The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural-glial networks,” Philos. Trans. R. Soc., B 370(1672), 20140183 (2015).
[Crossref]

K. Fuxe, D. O. Borroto-Escuela, W. Romero-Fernandez, Z. Diaz-Cabiale, A. Rivera, L. Ferraro, S. Tanganelli, A. O. Tarakanov, P. Garriga, J. A. Narváez, F. Ciruela, M. Guescini, and L. F. Agnati, “Extrasynaptic neurotransmission in the modulation of brain function. focus on the striatal neuronal-glial networks,” Front. Physio. 3, 136 (2012).
[Crossref]

K. Fuxe, S. Ferré, S. Genedani, R. Franco, and L. F. Agnati, “Adenosine receptor-dopamine receptor interactions in the basal ganglia and their relevance for brain function,” Physiol. Behav. 92(1-2), 210–217 (2007).
[Crossref]

Alfano, R.

L. Shi, L. A. Sordillo, A. Rodríguez-Contreras, and R. Alfano, “Transmission in near-infrared optical windows for deep brain imaging,” J. Biophotonics 9(1-2), 38–43 (2016).
[Crossref]

Allen, R.

M. L. Gostkowski, R. Allen, M. L. Plenert, E. Okerberg, M. J. Gordon, and J. B. Shear, “Multiphoton-excited serotonin photochemistry,” Biophys. J. 86(5), 3223–3229 (2004).
[Crossref]

Aoyagi, Y.

Y. Aoyagi, R. Kawakami, H. Osanai, T. Hibi, and T. Nemoto, “A rapid optical clearing protocol using 2,2’-thiodiethanol for microscopic observation of fixed mouse brain,” PLoS One 21, 081205 (2015).
[Crossref]

Arumugam, S.

S. K. Kaushalya, R. Desai, S. Arumugam, H. Ghosh, J. Balaji, and S. Maiti, “Three-photon microscopy shows that somatic release can be a quantitatively significant component of serotonergic neurotransmission in the mammalian brain,” J. Neurosci. Res. 86(15), 3469–3480 (2008).
[Crossref]

Baccus, S.

M. Menz, F. F. De-Miguel, and S. Baccus, Instituto de Fisiología Celular-Neurociencias, Universidad Nacional Autónoma de México. Circuito Exterior, Ciudad Universitaria, 04510, D. F., México. are preparing a manuscript to be called "Release of serotonin from the neuronal soma visualize upon multiphoton excitation".

Balaji, J.

S. K. Kaushalya, R. Desai, S. Arumugam, H. Ghosh, J. Balaji, and S. Maiti, “Three-photon microscopy shows that somatic release can be a quantitatively significant component of serotonergic neurotransmission in the mammalian brain,” J. Neurosci. Res. 86(15), 3469–3480 (2008).
[Crossref]

S. K. Kaushalya, S. Nag, J. Balaji, and S. Maiti, “Serotonin multiphoton imaging and relevant spectral data,” Proc. SPIE 6860, 68601C (2008).
[Crossref]

J. Balaji, R. Desai, S. K. Kaushalya, M. J. Eaton, and S. Maiti, “Quantitative measurement of serotonin synthesis and sequestration in individual live neuronal cells,” J. Neurochem. 95(5), 1217–1226 (2005).
[Crossref]

J. Balaji, R. Desai, and S. Maiti, “Live cell ultraviolet microscopy: A comparison between two- and three-photon excitation,” Microsc. Res. Tech. 63(1), 67–71 (2004).
[Crossref]

Bechter, K.

D. O. Borroto-Escuela, L. F. Agnati, K. Bechter, A. Jansson, A. O. Tarakanov, and K. Fuxe, “The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural-glial networks,” Philos. Trans. R. Soc., B 370(1672), 20140183 (2015).
[Crossref]

Belmer, A.

E. Quentin, A. Belmer, and L. Maroteaux, “Somato-dendritic regulation of raphe serotonin neurons; a key to antidepressant action,” Front. Neurosci. 12, 982 (2018).
[Crossref]

Bindra, K.

K. Bindra, C. Singh, S. Oak, R. Sailaja, and P. Bisht, “Effect of nonlinear absorption in estimation of order of nonlinear optical process by fluorescence intensity,” Opt. Laser Technol. 43(8), 1486–1490 (2011).
[Crossref]

Bisht, P.

K. Bindra, C. Singh, S. Oak, R. Sailaja, and P. Bisht, “Effect of nonlinear absorption in estimation of order of nonlinear optical process by fluorescence intensity,” Opt. Laser Technol. 43(8), 1486–1490 (2011).
[Crossref]

Bogdanski, D. F.

S. Udenfriend, D. F. Bogdanski, and W. Herbert, “Fluorescence characteristics of 5-hydroxytryptamine (serotonin),” Science 122(3177), 972–973 (1955).
[Crossref]

Borroto-Escuela, D. O.

D. O. Borroto-Escuela, L. F. Agnati, K. Bechter, A. Jansson, A. O. Tarakanov, and K. Fuxe, “The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural-glial networks,” Philos. Trans. R. Soc., B 370(1672), 20140183 (2015).
[Crossref]

K. Fuxe, D. O. Borroto-Escuela, W. Romero-Fernandez, Z. Diaz-Cabiale, A. Rivera, L. Ferraro, S. Tanganelli, A. O. Tarakanov, P. Garriga, J. A. Narváez, F. Ciruela, M. Guescini, and L. F. Agnati, “Extrasynaptic neurotransmission in the modulation of brain function. focus on the striatal neuronal-glial networks,” Front. Physio. 3, 136 (2012).
[Crossref]

Bowman, R. L.

D. E. Duggan, R. L. Bowman, B. B. Brodie, and S. Udenfriend, “A spectrophotofluorometric study of compounds of biological interest,” Arch. Biochem. Biophys. 68(1), 1–14 (1957).
[Crossref]

Brodie, B. B.

D. E. Duggan, R. L. Bowman, B. B. Brodie, and S. Udenfriend, “A spectrophotofluorometric study of compounds of biological interest,” Arch. Biochem. Biophys. 68(1), 1–14 (1957).
[Crossref]

Bruns, D.

D. Bruns, D. Riedel, J. Klingauf, and R. Jahn, “Quantal release of serotonin,” Neuron 28(1), 205–220 (2000).
[Crossref]

Bunin, M. A.

M. A. Bunin and R. M. Wightman, “Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission,” J. Neurosci. 18(13), 4854–4860 (1998).
[Crossref]

Campagnola, P. J.

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A. K. Das, B. K. Maity, D. Surendran, U. Tripathy, and S. Maiti, “Label-free ratiometric imaging of serotonin in live cells,” ACS Chem. Neurosci. 8(11), 2369–2373 (2017).
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E. Del-bel, F. F. De-miguel, and M. E. Rice, “Extrasynaptic neurotransmission mediated by exocytosis and diffusive release of transmitter substances,” Front. Synaptic Neurosci. 10, 13 (2018).
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F. F. De-Miguel and J. G. Nicholls, “Release of chemical transmitters from cell bodies and dendrites of nerve cells,” Philos. Trans. R. Soc., B 370(1672), 20140181 (2015).
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M. Menz, F. F. De-Miguel, and S. Baccus, Instituto de Fisiología Celular-Neurociencias, Universidad Nacional Autónoma de México. Circuito Exterior, Ciudad Universitaria, 04510, D. F., México. are preparing a manuscript to be called "Release of serotonin from the neuronal soma visualize upon multiphoton excitation".

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S. K. Kaushalya, R. Desai, S. Arumugam, H. Ghosh, J. Balaji, and S. Maiti, “Three-photon microscopy shows that somatic release can be a quantitatively significant component of serotonergic neurotransmission in the mammalian brain,” J. Neurosci. Res. 86(15), 3469–3480 (2008).
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K. Fuxe, D. O. Borroto-Escuela, W. Romero-Fernandez, Z. Diaz-Cabiale, A. Rivera, L. Ferraro, S. Tanganelli, A. O. Tarakanov, P. Garriga, J. A. Narváez, F. Ciruela, M. Guescini, and L. F. Agnati, “Extrasynaptic neurotransmission in the modulation of brain function. focus on the striatal neuronal-glial networks,” Front. Physio. 3, 136 (2012).
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K. Fuxe, S. Ferré, S. Genedani, R. Franco, and L. F. Agnati, “Adenosine receptor-dopamine receptor interactions in the basal ganglia and their relevance for brain function,” Physiol. Behav. 92(1-2), 210–217 (2007).
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D. O. Borroto-Escuela, L. F. Agnati, K. Bechter, A. Jansson, A. O. Tarakanov, and K. Fuxe, “The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural-glial networks,” Philos. Trans. R. Soc., B 370(1672), 20140183 (2015).
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K. Fuxe, D. O. Borroto-Escuela, W. Romero-Fernandez, Z. Diaz-Cabiale, A. Rivera, L. Ferraro, S. Tanganelli, A. O. Tarakanov, P. Garriga, J. A. Narváez, F. Ciruela, M. Guescini, and L. F. Agnati, “Extrasynaptic neurotransmission in the modulation of brain function. focus on the striatal neuronal-glial networks,” Front. Physio. 3, 136 (2012).
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K. Fuxe, S. Ferré, S. Genedani, R. Franco, and L. F. Agnati, “Adenosine receptor-dopamine receptor interactions in the basal ganglia and their relevance for brain function,” Physiol. Behav. 92(1-2), 210–217 (2007).
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K. Fuxe, D. O. Borroto-Escuela, W. Romero-Fernandez, Z. Diaz-Cabiale, A. Rivera, L. Ferraro, S. Tanganelli, A. O. Tarakanov, P. Garriga, J. A. Narváez, F. Ciruela, M. Guescini, and L. F. Agnati, “Extrasynaptic neurotransmission in the modulation of brain function. focus on the striatal neuronal-glial networks,” Front. Physio. 3, 136 (2012).
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K. Fuxe, S. Ferré, S. Genedani, R. Franco, and L. F. Agnati, “Adenosine receptor-dopamine receptor interactions in the basal ganglia and their relevance for brain function,” Physiol. Behav. 92(1-2), 210–217 (2007).
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S. K. Kaushalya, R. Desai, S. Arumugam, H. Ghosh, J. Balaji, and S. Maiti, “Three-photon microscopy shows that somatic release can be a quantitatively significant component of serotonergic neurotransmission in the mammalian brain,” J. Neurosci. Res. 86(15), 3469–3480 (2008).
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M. L. Gostkowski, R. Allen, M. L. Plenert, E. Okerberg, M. J. Gordon, and J. B. Shear, “Multiphoton-excited serotonin photochemistry,” Biophys. J. 86(5), 3223–3229 (2004).
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M. L. Gostkowski, T. E. Curey, E. Okerberg, T. J. Kang, D. A. Vanden Bout, and J. B. Shear, “Effects of molecular oxygen on multiphoton-excited photochemical analysis of hydroxyindoles,” Anal. Chem. 72(16), 3821–3825 (2000).
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K. Fuxe, D. O. Borroto-Escuela, W. Romero-Fernandez, Z. Diaz-Cabiale, A. Rivera, L. Ferraro, S. Tanganelli, A. O. Tarakanov, P. Garriga, J. A. Narváez, F. Ciruela, M. Guescini, and L. F. Agnati, “Extrasynaptic neurotransmission in the modulation of brain function. focus on the striatal neuronal-glial networks,” Front. Physio. 3, 136 (2012).
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Y. Aoyagi, R. Kawakami, H. Osanai, T. Hibi, and T. Nemoto, “A rapid optical clearing protocol using 2,2’-thiodiethanol for microscopic observation of fixed mouse brain,” PLoS One 21, 081205 (2015).
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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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R. Tomer, L. Ye, B. Hsueh, and K. Deisseroth, “Advanced clarity for rapid and high-resolution imaging of intact tissues,” Nat. Protoc. 9(7), 1682–1697 (2014).
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D. Bruns, D. Riedel, J. Klingauf, and R. Jahn, “Quantal release of serotonin,” Neuron 28(1), 205–220 (2000).
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D. O. Borroto-Escuela, L. F. Agnati, K. Bechter, A. Jansson, A. O. Tarakanov, and K. Fuxe, “The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural-glial networks,” Philos. Trans. R. Soc., B 370(1672), 20140183 (2015).
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M. L. Gostkowski, T. E. Curey, E. Okerberg, T. J. Kang, D. A. Vanden Bout, and J. B. Shear, “Effects of molecular oxygen on multiphoton-excited photochemical analysis of hydroxyindoles,” Anal. Chem. 72(16), 3821–3825 (2000).
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S. K. Kaushalya, R. Desai, S. Arumugam, H. Ghosh, J. Balaji, and S. Maiti, “Three-photon microscopy shows that somatic release can be a quantitatively significant component of serotonergic neurotransmission in the mammalian brain,” J. Neurosci. Res. 86(15), 3469–3480 (2008).
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S. K. Kaushalya, S. Nag, J. Balaji, and S. Maiti, “Serotonin multiphoton imaging and relevant spectral data,” Proc. SPIE 6860, 68601C (2008).
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J. Balaji, R. Desai, S. K. Kaushalya, M. J. Eaton, and S. Maiti, “Quantitative measurement of serotonin synthesis and sequestration in individual live neuronal cells,” J. Neurochem. 95(5), 1217–1226 (2005).
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S. K. Kaushalya and S. Maiti, Quantitative Imaging of Serotonin Autofluorescence with Multiphoton Microscopy (CRC Press/Taylor & Francis, 2007).

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Y. Aoyagi, R. Kawakami, H. Osanai, T. Hibi, and T. Nemoto, “A rapid optical clearing protocol using 2,2’-thiodiethanol for microscopic observation of fixed mouse brain,” PLoS One 21, 081205 (2015).
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D. Bruns, D. Riedel, J. Klingauf, and R. Jahn, “Quantal release of serotonin,” Neuron 28(1), 205–220 (2000).
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M. W. Klymkowsky and J. Hanken, Whole-Mount Staining of Xenopus and Other Vertebrates (Elsevier, 1991).

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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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[Crossref]

Loew, L. M.

P. J. Campagnola, H. A. Clark, W. A. Mohler, A. Lewis, and L. M. Loew, “Second-harmonic imaging microscopy of living cells,” J. Biomed. Opt. 6(3), 277–286 (2001).
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Maiti, S.

B. K. Maity and S. Maiti, “Label-free imaging of neurotransmitters in live brain tissue by multi-photon ultraviolet microscopy,” Neuronal Signaling 2(4), NS20180132 (2018).
[Crossref]

A. K. Das, B. K. Maity, D. Surendran, U. Tripathy, and S. Maiti, “Label-free ratiometric imaging of serotonin in live cells,” ACS Chem. Neurosci. 8(11), 2369–2373 (2017).
[Crossref]

S. K. Kaushalya, R. Desai, S. Arumugam, H. Ghosh, J. Balaji, and S. Maiti, “Three-photon microscopy shows that somatic release can be a quantitatively significant component of serotonergic neurotransmission in the mammalian brain,” J. Neurosci. Res. 86(15), 3469–3480 (2008).
[Crossref]

S. K. Kaushalya, S. Nag, J. Balaji, and S. Maiti, “Serotonin multiphoton imaging and relevant spectral data,” Proc. SPIE 6860, 68601C (2008).
[Crossref]

J. Balaji, R. Desai, S. K. Kaushalya, M. J. Eaton, and S. Maiti, “Quantitative measurement of serotonin synthesis and sequestration in individual live neuronal cells,” J. Neurochem. 95(5), 1217–1226 (2005).
[Crossref]

J. Balaji, R. Desai, and S. Maiti, “Live cell ultraviolet microscopy: A comparison between two- and three-photon excitation,” Microsc. Res. Tech. 63(1), 67–71 (2004).
[Crossref]

R. M. Williams, J. B. Shear, W. R. Zipfel, S. Maiti, and W. W. Webb, “Mucosal mast cell secretion processes imaged using three-photon microscopy of 5-hydroxytryptamine autofluorescence,” Biophys. J. 76(4), 1835–1846 (1999).
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S. Maiti, J. B. Shear, R. M. Williams, W. R. Zipfel, and W. W. Webb, “Measuring serotonin distribution in live cells with three-photon excitation,” Science 275(5299), 530–532 (1997).
[Crossref]

S. K. Kaushalya and S. Maiti, Quantitative Imaging of Serotonin Autofluorescence with Multiphoton Microscopy (CRC Press/Taylor & Francis, 2007).

Maity, B. K.

B. K. Maity and S. Maiti, “Label-free imaging of neurotransmitters in live brain tissue by multi-photon ultraviolet microscopy,” Neuronal Signaling 2(4), NS20180132 (2018).
[Crossref]

A. K. Das, B. K. Maity, D. Surendran, U. Tripathy, and S. Maiti, “Label-free ratiometric imaging of serotonin in live cells,” ACS Chem. Neurosci. 8(11), 2369–2373 (2017).
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E. Quentin, A. Belmer, and L. Maroteaux, “Somato-dendritic regulation of raphe serotonin neurons; a key to antidepressant action,” Front. Neurosci. 12, 982 (2018).
[Crossref]

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M. Menz, F. F. De-Miguel, and S. Baccus, Instituto de Fisiología Celular-Neurociencias, Universidad Nacional Autónoma de México. Circuito Exterior, Ciudad Universitaria, 04510, D. F., México. are preparing a manuscript to be called "Release of serotonin from the neuronal soma visualize upon multiphoton excitation".

Mohler, W. A.

P. J. Campagnola, H. A. Clark, W. A. Mohler, A. Lewis, and L. M. Loew, “Second-harmonic imaging microscopy of living cells,” J. Biomed. Opt. 6(3), 277–286 (2001).
[Crossref]

Mukherjee, S.

A. Chattopadhyay, R. Rukmini, and S. Mukherjee, “Photophysics of a neurotransmitter: ionization and spectroscopic properties of serotonin,” Biophys. J. 71(4), 1952–1960 (1996).
[Crossref]

Nag, S.

S. K. Kaushalya, S. Nag, J. Balaji, and S. Maiti, “Serotonin multiphoton imaging and relevant spectral data,” Proc. SPIE 6860, 68601C (2008).
[Crossref]

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K. Fuxe, D. O. Borroto-Escuela, W. Romero-Fernandez, Z. Diaz-Cabiale, A. Rivera, L. Ferraro, S. Tanganelli, A. O. Tarakanov, P. Garriga, J. A. Narváez, F. Ciruela, M. Guescini, and L. F. Agnati, “Extrasynaptic neurotransmission in the modulation of brain function. focus on the striatal neuronal-glial networks,” Front. Physio. 3, 136 (2012).
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Y. Aoyagi, R. Kawakami, H. Osanai, T. Hibi, and T. Nemoto, “A rapid optical clearing protocol using 2,2’-thiodiethanol for microscopic observation of fixed mouse brain,” PLoS One 21, 081205 (2015).
[Crossref]

Nicholls, J. G.

F. F. De-Miguel and J. G. Nicholls, “Release of chemical transmitters from cell bodies and dendrites of nerve cells,” Philos. Trans. R. Soc., B 370(1672), 20140181 (2015).
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Oak, S.

K. Bindra, C. Singh, S. Oak, R. Sailaja, and P. Bisht, “Effect of nonlinear absorption in estimation of order of nonlinear optical process by fluorescence intensity,” Opt. Laser Technol. 43(8), 1486–1490 (2011).
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Okerberg, E.

M. L. Gostkowski, R. Allen, M. L. Plenert, E. Okerberg, M. J. Gordon, and J. B. Shear, “Multiphoton-excited serotonin photochemistry,” Biophys. J. 86(5), 3223–3229 (2004).
[Crossref]

M. L. Gostkowski, T. E. Curey, E. Okerberg, T. J. Kang, D. A. Vanden Bout, and J. B. Shear, “Effects of molecular oxygen on multiphoton-excited photochemical analysis of hydroxyindoles,” Anal. Chem. 72(16), 3821–3825 (2000).
[Crossref]

Osanai, H.

Y. Aoyagi, R. Kawakami, H. Osanai, T. Hibi, and T. Nemoto, “A rapid optical clearing protocol using 2,2’-thiodiethanol for microscopic observation of fixed mouse brain,” PLoS One 21, 081205 (2015).
[Crossref]

Pavone, F. S.

L. Silvestri, I. Costantini, L. Sacconi, and F. S. Pavone, “Clearing of fixed tissue: a review from a microscopist’s perspective,” J. Biomed. Opt. 21(8), 081205 (2016).
[Crossref]

Plenert, M. L.

M. L. Gostkowski, R. Allen, M. L. Plenert, E. Okerberg, M. J. Gordon, and J. B. Shear, “Multiphoton-excited serotonin photochemistry,” Biophys. J. 86(5), 3223–3229 (2004).
[Crossref]

Quentin, E.

E. Quentin, A. Belmer, and L. Maroteaux, “Somato-dendritic regulation of raphe serotonin neurons; a key to antidepressant action,” Front. Neurosci. 12, 982 (2018).
[Crossref]

Rice, M. E.

E. Del-bel, F. F. De-miguel, and M. E. Rice, “Extrasynaptic neurotransmission mediated by exocytosis and diffusive release of transmitter substances,” Front. Synaptic Neurosci. 10, 13 (2018).
[Crossref]

Riedel, D.

D. Bruns, D. Riedel, J. Klingauf, and R. Jahn, “Quantal release of serotonin,” Neuron 28(1), 205–220 (2000).
[Crossref]

Rivera, A.

K. Fuxe, D. O. Borroto-Escuela, W. Romero-Fernandez, Z. Diaz-Cabiale, A. Rivera, L. Ferraro, S. Tanganelli, A. O. Tarakanov, P. Garriga, J. A. Narváez, F. Ciruela, M. Guescini, and L. F. Agnati, “Extrasynaptic neurotransmission in the modulation of brain function. focus on the striatal neuronal-glial networks,” Front. Physio. 3, 136 (2012).
[Crossref]

Rodríguez-Contreras, A.

L. Shi, L. A. Sordillo, A. Rodríguez-Contreras, and R. Alfano, “Transmission in near-infrared optical windows for deep brain imaging,” J. Biophotonics 9(1-2), 38–43 (2016).
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K. Fuxe, D. O. Borroto-Escuela, W. Romero-Fernandez, Z. Diaz-Cabiale, A. Rivera, L. Ferraro, S. Tanganelli, A. O. Tarakanov, P. Garriga, J. A. Narváez, F. Ciruela, M. Guescini, and L. F. Agnati, “Extrasynaptic neurotransmission in the modulation of brain function. focus on the striatal neuronal-glial networks,” Front. Physio. 3, 136 (2012).
[Crossref]

Rukmini, R.

A. Chattopadhyay, R. Rukmini, and S. Mukherjee, “Photophysics of a neurotransmitter: ionization and spectroscopic properties of serotonin,” Biophys. J. 71(4), 1952–1960 (1996).
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Sacconi, L.

L. Silvestri, I. Costantini, L. Sacconi, and F. S. Pavone, “Clearing of fixed tissue: a review from a microscopist’s perspective,” J. Biomed. Opt. 21(8), 081205 (2016).
[Crossref]

Sailaja, R.

K. Bindra, C. Singh, S. Oak, R. Sailaja, and P. Bisht, “Effect of nonlinear absorption in estimation of order of nonlinear optical process by fluorescence intensity,” Opt. Laser Technol. 43(8), 1486–1490 (2011).
[Crossref]

Schaffer, C. B.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[Crossref]

Shear, J. B.

M. L. Gostkowski, R. Allen, M. L. Plenert, E. Okerberg, M. J. Gordon, and J. B. Shear, “Multiphoton-excited serotonin photochemistry,” Biophys. J. 86(5), 3223–3229 (2004).
[Crossref]

M. L. Gostkowski, T. E. Curey, E. Okerberg, T. J. Kang, D. A. Vanden Bout, and J. B. Shear, “Effects of molecular oxygen on multiphoton-excited photochemical analysis of hydroxyindoles,” Anal. Chem. 72(16), 3821–3825 (2000).
[Crossref]

R. M. Williams, J. B. Shear, W. R. Zipfel, S. Maiti, and W. W. Webb, “Mucosal mast cell secretion processes imaged using three-photon microscopy of 5-hydroxytryptamine autofluorescence,” Biophys. J. 76(4), 1835–1846 (1999).
[Crossref]

S. Maiti, J. B. Shear, R. M. Williams, W. R. Zipfel, and W. W. Webb, “Measuring serotonin distribution in live cells with three-photon excitation,” Science 275(5299), 530–532 (1997).
[Crossref]

J. B. Shear, C. Xu, and W. W. Webb, “Multiphoton-excited visible emission by serotonin solutions,” Photochem. Photobiol. 65(6), 931–936 (1997).
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Shi, L.

L. Shi, L. A. Sordillo, A. Rodríguez-Contreras, and R. Alfano, “Transmission in near-infrared optical windows for deep brain imaging,” J. Biophotonics 9(1-2), 38–43 (2016).
[Crossref]

Silvestri, L.

L. Silvestri, I. Costantini, L. Sacconi, and F. S. Pavone, “Clearing of fixed tissue: a review from a microscopist’s perspective,” J. Biomed. Opt. 21(8), 081205 (2016).
[Crossref]

Singh, C.

K. Bindra, C. Singh, S. Oak, R. Sailaja, and P. Bisht, “Effect of nonlinear absorption in estimation of order of nonlinear optical process by fluorescence intensity,” Opt. Laser Technol. 43(8), 1486–1490 (2011).
[Crossref]

Sordillo, L. A.

L. Shi, L. A. Sordillo, A. Rodríguez-Contreras, and R. Alfano, “Transmission in near-infrared optical windows for deep brain imaging,” J. Biophotonics 9(1-2), 38–43 (2016).
[Crossref]

Surendran, D.

A. K. Das, B. K. Maity, D. Surendran, U. Tripathy, and S. Maiti, “Label-free ratiometric imaging of serotonin in live cells,” ACS Chem. Neurosci. 8(11), 2369–2373 (2017).
[Crossref]

Tanaka, J.

T. Kishi, M. Tanaka, and J. Tanaka, “Electronic absorption and fluorescence spectra of 5-hydroxytryptamine (serotonin). protonation in the excited state,” Bull. Chem. Soc. Jpn. 50(5), 1267–1271 (1977).
[Crossref]

Tanaka, M.

T. Kishi, M. Tanaka, and J. Tanaka, “Electronic absorption and fluorescence spectra of 5-hydroxytryptamine (serotonin). protonation in the excited state,” Bull. Chem. Soc. Jpn. 50(5), 1267–1271 (1977).
[Crossref]

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K. Fuxe, D. O. Borroto-Escuela, W. Romero-Fernandez, Z. Diaz-Cabiale, A. Rivera, L. Ferraro, S. Tanganelli, A. O. Tarakanov, P. Garriga, J. A. Narváez, F. Ciruela, M. Guescini, and L. F. Agnati, “Extrasynaptic neurotransmission in the modulation of brain function. focus on the striatal neuronal-glial networks,” Front. Physio. 3, 136 (2012).
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Tarakanov, A. O.

D. O. Borroto-Escuela, L. F. Agnati, K. Bechter, A. Jansson, A. O. Tarakanov, and K. Fuxe, “The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural-glial networks,” Philos. Trans. R. Soc., B 370(1672), 20140183 (2015).
[Crossref]

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R. Tomer, L. Ye, B. Hsueh, and K. Deisseroth, “Advanced clarity for rapid and high-resolution imaging of intact tissues,” Nat. Protoc. 9(7), 1682–1697 (2014).
[Crossref]

Tripathy, U.

A. K. Das, B. K. Maity, D. Surendran, U. Tripathy, and S. Maiti, “Label-free ratiometric imaging of serotonin in live cells,” ACS Chem. Neurosci. 8(11), 2369–2373 (2017).
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[Crossref]

S. Udenfriend, D. F. Bogdanski, and W. Herbert, “Fluorescence characteristics of 5-hydroxytryptamine (serotonin),” Science 122(3177), 972–973 (1955).
[Crossref]

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M. L. Gostkowski, T. E. Curey, E. Okerberg, T. J. Kang, D. A. Vanden Bout, and J. B. Shear, “Effects of molecular oxygen on multiphoton-excited photochemical analysis of hydroxyindoles,” Anal. Chem. 72(16), 3821–3825 (2000).
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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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R. Tomer, L. Ye, B. Hsueh, and K. Deisseroth, “Advanced clarity for rapid and high-resolution imaging of intact tissues,” Nat. Protoc. 9(7), 1682–1697 (2014).
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W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
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R. M. Williams, J. B. Shear, W. R. Zipfel, S. Maiti, and W. W. Webb, “Mucosal mast cell secretion processes imaged using three-photon microscopy of 5-hydroxytryptamine autofluorescence,” Biophys. J. 76(4), 1835–1846 (1999).
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S. Maiti, J. B. Shear, R. M. Williams, W. R. Zipfel, and W. W. Webb, “Measuring serotonin distribution in live cells with three-photon excitation,” Science 275(5299), 530–532 (1997).
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F. F. De-Miguel and C. Trueta, “Synaptic and extrasynaptic secretion of serotonin,” Cell. Mol. Neurobiol. 25(2), 297–312 (2005).
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L. Shi, L. A. Sordillo, A. Rodríguez-Contreras, and R. Alfano, “Transmission in near-infrared optical windows for deep brain imaging,” J. Biophotonics 9(1-2), 38–43 (2016).
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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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R. Tomer, L. Ye, B. Hsueh, and K. Deisseroth, “Advanced clarity for rapid and high-resolution imaging of intact tissues,” Nat. Protoc. 9(7), 1682–1697 (2014).
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K. Bindra, C. Singh, S. Oak, R. Sailaja, and P. Bisht, “Effect of nonlinear absorption in estimation of order of nonlinear optical process by fluorescence intensity,” Opt. Laser Technol. 43(8), 1486–1490 (2011).
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Science (2)

S. Maiti, J. B. Shear, R. M. Williams, W. R. Zipfel, and W. W. Webb, “Measuring serotonin distribution in live cells with three-photon excitation,” Science 275(5299), 530–532 (1997).
[Crossref]

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La.mathworks.com , “Singular spectrum analysis - beginners guide - file exchange - matlab central.” https://la.mathworks.com/matlabcentral/fileexchange/58967-singular-spectrum-analysis-beginners-guide . [retrieved 01 July 2019].

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M. Menz, F. F. De-Miguel, and S. Baccus, Instituto de Fisiología Celular-Neurociencias, Universidad Nacional Autónoma de México. Circuito Exterior, Ciudad Universitaria, 04510, D. F., México. are preparing a manuscript to be called "Release of serotonin from the neuronal soma visualize upon multiphoton excitation".

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Figures (13)

Fig. 1.
Fig. 1. Diagram of the excitation-acquisition system. A 1.0 numerical aperture objective focuses a femtosecond-pulsed laser on a drop of serotonin solution (Sample). The fluorescence is collected as transmitted light by a condenser lens. Infrared contamination is filtered with a saturated copper-sulfate (CuSO$_4$) filter. Rotation of the diffraction grating of the monochromator permitted to acquire the light emissions with 1 nm resolution. The signal was captured with a high-sensitivity PMT.
Fig. 2.
Fig. 2. Light intensity at the sample in TW/cm$^2$, calculated for each average laser power (right numbers in mW) as a function of the $\lambda _{\textrm {exc}}$(nm). The negative slope of the curves occurs because the area of the focal spot increases with $\lambda _{\textrm {exc}}$. Therefore, the intensity decreases.
Fig. 3.
Fig. 3. Absorption of serotonin at increasing concentrations (1.0, 3.0, 10.0, 30.0, 100.0 and 270.0 mM). The absorption wavelength was 250 nm. The plot shows a continuous increase in the absorption rate, thus confirming that even at the high 270 mM concentration, serotonin was well-diluted. The blue line links the average values of four measurements at each concentration; the dim blue background trace is the standard deviation, for informative purposes.
Fig. 4.
Fig. 4. Processing of data. Fluorescence spectrum ($\lambda _{\textrm {em}}$) of serotonin at a 270 mM concentration, $\lambda _{\textrm {exc}}=700$ nm and 60 mW laser power. The blue dots are the data after a correction for the efficiency of the acquisition devices. The orange line shows the data after being smoothed with 2 components of the SSA algorithm. Note the presence of a small fluorescence peak in the plot (arrow).
Fig. 5.
Fig. 5. Spectra of absorption and emission of serotonin upon monophotonic excitation. The serotonin concentration was 1 mM. The purple curve in the low wavelength range (left of the plot) is the absorption spectrum. The peaks in the region above the double bars were produced by saturation of the acquisition device. Illumination of the serotonin solution with wavelengths from 230 to 309 nm (arrows from a to d) produced similar fluorescence emissions (blue traces) with a peak at $\sim$340 nm and amplitudes, determined by the absorption wavelength.
Fig. 6.
Fig. 6. The fluorescence spectra ($\lambda _{\textrm {em}}$) depended on the excitation wavelength ($\lambda _{\textrm {exc}}$), power and serotonin concentration. The excitation wavelength is indicated in one of the axis. (A) Laser power-dependence of the emissions. Measurements were made using a high 270 mM serotonin concentration. The excitation powers are indicated in the inset. The violet and blue emissions appeared predominantly in response to $\lambda _{\textrm {exc}}$ from 690 to 720 nm. Note the reduced levels of green fluorescence obtained with $\lambda _{\textrm {exc}}$ of 710 and 730 nm. (B) Concentration-dependence of the fluorescent. Spectra were obtained at a fixed 60 mW excitation power. The serotonin concentrations are indicated in the inset. Note the discontinuities in the rate of increase of the spectra as the serotonin concentration was increased. The violet and blue emissions were more prominent at $\lambda _{\textrm {exc}}$ = 700 nm and concentrations of 100 and 270 mM.
Fig. 7.
Fig. 7. The serotonin fluorescence depended on the excitation wavelength, laser power and serotonin concentration. A) Fluorescence spectra ($\lambda _{\textrm {em}}$) of high (270 mM) serotonin concentration excited with the wavelengths ($\lambda _{\textrm {exc}}$) indicated on the top. The colors of the traces correspond to the laser powers in the inset. $\lambda _{\textrm {exc}}=700$ nm produced three emissions. The UV emission, indicated by the first arrow from left to right is partially masked by the blue emission (second arrow) and by the cutoff of the optical system at wavelengths below 350 nm. The largest emission appears in the green range of the spectrum. The fluorescence levels decayed with a $\lambda _{\textrm {exc}}=720$ nm and increased again in response to a $\lambda _{\textrm {exc}}=740$ nm. B) Fluorescence as a function of the laser power for the three excitation wavelengths in A. Each emission follows a different trend. Note that when $\lambda _{\textrm {exc}}$= 700 nm the blue emission was detected only at high powers, then was absent when $\lambda _{\textrm {exc}}$= 720 nm and reappeared in the whole power range when $\lambda _{\textrm {exc}}$= 740 nm. The slopes (m values) were obtained from the whole range of values in each plot. C) At a 60 mW laser power, the variations in the serotonin concentration changed the relative amplitudes of the three emissions. Note the non-linearities in the peak amplitudes of the emissions as the serotonin concentration was increased. The peak amplitudes of the green and violet emissions follow similar trends with quenching at high concentrations, while the blue emissions has an increase at this same 100 and 270 mM serotonin concentrations. Note also that the emissions at $\lambda _{\textrm {exc}}$= 700 and 740 nm are qualitatively similar although with different amplitudes. At the intermediate $\lambda _{\textrm {exc}}$= 720 nm the quenching of the green and violet emissions was enhanced while the increase in the blue emission was reduced. D) Maximum fluorescence as a function of the serotonin concentration at the three excitation wavelengths shown in C. Note the reduction of the rate of increase of the green and violet emissions as the serotonin concentration increases from 100 to 270 mM. By contrast, the blue emission was increased at those same concentrations.
Fig. 8.
Fig. 8. Quantitative representation of the fluorescence of serotonin as a dual function of the laser power and excitation wavelength. The triangle contains data from all at a emissions from a 270 mM concentration. The green levels are proportional to the peak amplitude of the spectrum in arbitrary units, as indicated in the scale bar on the bottom right. It may be seen that the green emission of serotonin at a 270 mM concentration was more intense in response to $\lambda _{\textrm {exc}}$ of 700 and 760 nm and at 55 and 60 mW laser powers. $\lambda _{\textrm {exc}}$ of 710 and 730 nm produced the dimmest emissions. Note that power lasers of 35 and 45 mW produced higher intensity than their immediate higher steps. This plot is the building block of the heptagons in Fig. 9, which are complemented with the information from the six other serotonin concentrations tested arranged in an increasing manner, as indicated by the arrow in the bottom left of this Figure.
Fig. 9.
Fig. 9. Quantitative comparison of the three fluorescence emissions of serotonin. Each triangle in the heptagon contains the wavelength- and power-dependence of the fluorescence emission of one serotonin concentration (mM) as indicated in the brackets. The emissions were measured at 373 nm (violet), 405 nm (blue) and 494 nm (green). The arrow in the violet heptagon indicates the increasing order of the serotonin concentrations. The intensity of the color is proportional to the fluorescence intensity, according to the scale bars below each heptagon, which are in arbitrary units. The most efficient excitation wavelength to generate the triple emission was 700 nm (asterisks). It can be seen that due to the non-linearities in the concentration dependence of the emissions, the blue emission in response to a 40 mW laser power could be well-resolved. The lack of fluorescence at concentrations below 30 mM can be attributed to the low sensitivity of our spectroscopic device.
Fig. 10.
Fig. 10. Absorption and emission spectra of the blue emission in response to photoconversion of serotonin. (A) A sustained 30 minute irradiation of a 0.3 mM serotonin solution with 700 nm at 60 mW produced a tail in the low energy range of the absorption spectrum of the serotonin solution, from $\sim$310 to $\sim$360 nm. The inset shows an amplified segment of the absorption spectrum displaying the tail in the absorption. The dashed line indicates the low value of the absorption. (B) Excitation of the serotonin sample at 350 nm generated blue fluorescence with a $\sim$390 nm peak (blue trace). Such emission was absent from the serotonin emission spectrum generated by a 320 nm UV excitation light (violet trace).
Fig. 11.
Fig. 11. Excitation-wavelength-dependence of the blue fluorescence. The serotonin sample was irradiated for 30 minutes with 700, 710 or 720 nm. The maximum amplitude of the $\sim$390 peak was proportional to the efficiency of the irradiation wavelength to produce blue fluorescence shown in Fig. 7. The asterisks mark a smaller green emission with a peak by 470 nm (single asterisks) and yet another smaller green-yellow emission with a peak at $\sim$540 nm (double asterisk). Similar green-yellow peaks appeared in the spectrum of the control solution (grey trace at the bottom).
Fig. 12.
Fig. 12. Biphotonic excitation of irradiated serotonin produces the blue fluorescence. A solution containing 100 mM of 5-HT was irradiated for 30 min with 700 nm at 60 mW. The emission spectrum was tested in response to biphotonic excitation with 700 nm. The green trace is the spectrum of the solution before irradiation and the blue trace is after irradiation. The arrow indicates the 405 nm peak of the blue emission. An increase in the peak of green emission appeared after irradiation.
Fig. 13.
Fig. 13. Direct and indirect emissions of serotonin in response to multiphoton excitation. The excitation spectrum and the three multiphoton emissions of serotonin are superimposed. The absorption spectrum is purple. The bar with the arrows indicates the region of the spectrum excited with three photons in this study. The dim traces above the double bars appear saturated due to the high resolution of the measuring equipment. The violet trace is the UV fluorescence produced by mono or multiphoton absorption. The dotted trace that follows the purple emission is the absorption spectrum of the blue-emitting photoproduct. The arrow indicates the absorption wavelength of the mono-and multiphoton excitation in our experiments. The blue spectrum was obtained from irradiated solutions excited monophotonically. On the right is the green emission spectrum. The approximate peak values are indicated in each spectrum. The amplitude of the spectra are normalized to the 494 nm maximum. Data are in arbitrary units.

Tables (2)

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Table 1. Area of the focal spot for each excitation wavelength used here

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Table 2. Multiphotonic excitation and emission wavelengths of the blue and green fluorescence serotonin emissions in this study.

Equations (1)

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I = P a v g f r a t e τ p u l s e A s p o t

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