Neuroenergetics
Frontiers in Neuroenergetics ·
Volume 2 - 2010 | https://doi.org/10.3389/fnene.2010.00021
Multi-Photon Nanosurgery in Live Brain
- Anna Letizia Allegra Mascaro1
- Leonardo Sacconi1,2
- Francesco S. Pavone1,2*corresponding author
- 11 European Laboratory for Non-linear Spectroscopy, University of Florence Florence, Italy
- 22 Department of Physics, University of Florence Florence, Italy
Abstract
In the last few years two-photon microscopy has been used to perform in vivo high spatial resolution imaging of neurons, glial cells and vascular structures in the intact neocortex. Recently, in parallel to its applications in imaging, multi-photon absorption has been used as a tool for the selective disruption of neural processes and blood vessels in living animals. In this review we present some basic features of multi-photon nanosurgery and we illustrate the advantages offered by this novel methodology in neuroscience research. We show how the spatial localization of multi-photon excitation can be exploited to perform selective lesions on cortical neurons in living mice expressing fluorescent proteins. This methodology is applied to disrupt a single neuron without causing any visible collateral damage to the surrounding structures. The spatial precision of this method allows to dissect single processes as well as individual dendritic spines, preserving the structural integrity of the main neuronal arbor. The same approach can be used to breach the blood-brain barrier through a targeted photo-disruption of blood vessels walls. We show how the vascular system can be perturbed through laser ablation leading toward two different models of stroke: intravascular clot and extravasation. Following the temporal evolution of the injured system (either a neuron or a blood vessel) through time lapse in vivo imaging, the physiological response of the target structure and the rearrangement of the surrounding area can be characterized. Multi-photon nanosurgery in live brain represents a useful tool to produce different models of neurodegenerative disease.
Keywords
References
- Balaban C. D. (1985). Central neurotoxic effects of intraperitoneally administered 3-acetylpyridine, harmaline and niacinamide in Sprague-Dawley and Long-Evans rats: a critical review of central 3-acetylpyridine neurotoxicity. Brain Res. 356, 21 – 42.
- Chen S. T., Hsu C. Y., Hogan E. L., Maricq H., Balentine J. D. (1986). A model of focal ischemic stroke in the rat: reproducible extensive cortical infarction. Stroke 17, 738 – 743.
- Chung S. H., Clark D. A., Gabel C. V., Mazur E., Samuel A. D. (2006). The role of the AFD neuron in C. elegans thermotaxis analyzed using femtosecond laser ablation. BMC Neurosci. 7, 30. doi:10.1186/1471-2202-7-30
- Cullen K. M., Kócsi Z., Stone J. (2005). Pericapillary haem-rich deposits: evidence for microhaemorrhages in aging human cerebral cortex. J. Cereb. Blood Flow Metab. 25, 1656 – 1667. doi:10.1038/sj.jcbfm.9600155
- Davalos D., Grutzendler J., Yang G., Kim J. V., Zuo Y., Jung S., Littman D. R., Dustin M. L., Gan W. B. (2005). ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8, 752 – 758. doi:10.1038/nn1472
- Denk W., Strickler H. J., Webb W. W. (1990). Two-photon laser scanning fluorescence microscopy. Science 248, 73 – 76. doi:10.1126/science.2321027
- Desclina J. C., Escubia J. (1974). Effects of 3-acetylpyridine on the central nervous system of the rat, as demonstrated by silver methods. Brain Res. 77, 349 – 364. doi:10.1016/0006-8993(74)90627-1
- George R., Griffin J. W. (1994). Delayed macrophage responses and myelin clearance during Wallerian degeneration in the central nervous system: the dorsal radiculotomy model. Exp. Neurol. 129, 225 – 236. doi:10.1006/exnr.1994.1164
- Gold G., Giannakopoulos P., Herrmann F. R., Bouras C., Kövari E. (2007). Identification of Alzheimer and vascular lesion thresholds for mixed dementia. Brain 130, 2830. doi:10.1093/brain/awm228
- Grutzendler J., Kasthuri N., Gan W. B. (2002). Long-term dendritic spine stability in the adult cortex. Nature 420, 812 – 816. doi:10.1038/nature01276
- Heisterkamp A., Maxwell I. Z., Mazur E., Underwood J. M., Nickerson J. A., Kumar S., Ingber D. E. (2005). Pulse energy dependence of subcellular dissection by femtosecond laser pulses. Opt. Express 13, 3690 – 3696. doi:10.1364/OPEX.13.003690
- Helmchen F., Denk W. (2005). Deep tissue two-photon microscopy. Nat. Methods 2, 932 – 940. doi:10.1038/nmeth818
- Hicks S. P. (1955). Pathologic effects of antimetabolites. I. Acute lesions in the hypothalamus, peripheral ganglia, and adrenal medulla caused by 3-acetyl pyridine and prevented by nicotinamide. Am. J. Pathol. 31, 189 – 199.
- Holtmaat A., Bonhoeffer T., Chow D. K., Chuckowree J., De Paola V., Hofer S. B., Hübener M., Keck T., Knott G., Lee W. C., Mostany R., Mrsic-Flogel T. D., Nedivi E., Portera-Cailliau C., Svoboda K., Trachtenberg J. T., Wilbrecht L. (2009). Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 4, 1128 – 1144. doi:10.1038/nprot.2009.89
- Holtmaat A., Wilbrecht L., Knott G. W., Welker E., Svoboda K. (2006). Experience dependent and cell-type-specific spine growth in the neocortex. Nature 441, 979 – 983. doi:10.1038/nature04783
- Kerschensteiner M., Schwab M. E., Lichtman J. W., Misgeld T. (2005). In vivo imaging of axonal degeneration and regeneration in the injured spinal cord. Nat. Med. 11, 572 – 577. doi:10.1038/nm1229
- Kleinfeld D., Friedman B., Lyden P. D., Shih A. Y. (2008). “Targeted occlusion to surface and deep vessels in neocortex via linear and nonlinear optical absorption,” in Animal Models of acute Neurological Injuries, eds Chen J., Xu Z., Xu X.-M., Zhang J. (New York: The Humana Press Inc), pp. 169 – 185.
- Kleinfeld D., Mitra P. P., Helmchen F., Denk W. (1998). Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc. Natl. Acad. Sci. U.S.A. 95, 15741 – 15746. doi:10.1073/pnas.95.26.15741
- Kohli V., Elezzabi A. Y. (2008). Laser surgery of zebrafish (Danio rerio) embryos using femtosecond laser pulses: Optimal parameters for exogenous material delivery, and the laser's effect on short- and long-term development. BMC Biotechnol. 8, 7. doi:10.1186/1472-6750-8-7
- König K., Riemann I., Fritzsche W. (2001). Nanodissection of human chromosomes with near-infrared femtosecond laser pulses. Opt. Lett. 26, 819 – 821. doi:10.1364/OL.26.000819
- König K., Riemann I., Fischer P., Halbhuber K. H. (1999). Intracellular nanosurgery with near infrared femtosecond laser pulses. Cell. Mol. Biol. 45, 195 – 201.
- Kumar S., Maxwell I. Z., Heisterkamp A., Polte T. R., Lele T., Salanga M., Mazur E., Ingber D. E. (2006). Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys. J. 90, 3762 – 3773. doi:10.1529/biophysj.105.071506
- Lendvai B., Stern E., Chen B., Svoboda K. (2000). Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404, 876 – 881. doi:10.1038/35009107
- Li P., Murphy T. H. (2008). Two-Photon Imaging during Prolonged Middle Cerebral Artery Occlusion in Mice Reveals Recovery of Dendritic Structure after Reperfusion. J. Neurosci. 28, 11970 – 11979. doi:10.1523/JNEUROSCI.3724-08.2008
- Mostany R., Portera-Cailliau C. (2008). A craniotomy surgery procedure for chronic brain imaging. JoVE. (2008) Available at: http://www.jove.com/index/details.stp?id=680,. doi:10.3791/680
- Nimmerjahn A., Kirchhoff F., Helmchen F. (2005). Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314 – 1318. doi:10.1126/science.1110647
- Nishimura N., Schaffer C. B., Friedman B., Tsai P. S., Lyden P. D., Kleinfeld D. (2006). Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke. Nat. Methods 3, 99 – 108. doi:10.1038/nmeth844
- Oehring H., Riemann I., Fischer P., Halbhuber K. J., König K. (2000). Ultrastructure and reproduction behaviour of single CHO-K1 cells exposed to near infrared femtosecond laser pulses. Scanning 22, 263 – 270. doi:10.1002/sca.4950220406
- Sacconi L., O'Connor R. P., Jasaitis A., Masi A., Buffelli M., Pavone F. S. (2007). In vivo multi-photon nanosurgery on cortical neurons. J. Biomed. Opt. 12, 050502. doi:10.1117/1.2798723
- Sacconi L., Tolić-Nørrelykke I. M., Antolini R., Pavone F. S. (2005). Combined intracellular three-dimensional imaging and selective nanosurgery by a nonlinear microscope. J. Biomed. Opt. 10, 014002 – 014005. doi:10.1117/1.1854675
- Schaffer C. B., Friedman B., Nishimura N., Schroeder L. F., Tsai P. S., Ebner F. F., Lyden P. D., Kleinfeld D. (2006). Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol. 4, e22. doi:10.1371/journal.pbio.0040022
- Shen N., Datta D., Schaffer C. B., LeDuc P., Ingber D. E., Mazur E. (2005). Ablation of cytoskeletal filaments and mitochondria in cells using a femtosecond laser nanoscissor. Mech. Chem. Biosyst. 2, 17 – 26.
- Shimada T., Watanabe W., Matsunaga S., Higashi T., Ishii H., Fukui K., Isobe K., Itoh K. (2005). Intracellular disruption of mitochondria in a living HeLa cell with a 76-MHz femtosecond laser oscillator. Opt. Express 13, 9869 – 9880. doi:10.1364/OPEX.13.009869
- Smith N. I., Fujita K., Kaneko T., Katoh K., Nakamura O., Kawata S., Takamatsu T. (2001). Generation of calcium waves in living cells by pulsed-laser-induced photodisruption. Appl. Phys. Lett. 79, 1208 – 1210. doi:10.1063/1.1397255
- Supatto W., Débarre D., Moulia B., Brouzés E., Martin J., Farge E., Beaurepaire E. (2005). In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses. Proc. Natl. Acad. Sci. U.S.A. 102, 1047 – 1052. doi:10.1073/pnas.0405316102
- Supatto W., Fraser S. E., Vermot J. (2008). An all-optical approach for probing microscopic flows in living embryos. Biophys. J. 95, 4. doi:10.1529/biophysj.108.137786
- Svoboda K., Yasuda R. (2006). Principles of two-photon excitation microscopy and its applications to neuroscience. Neuron 50, 823 – 839. doi:10.1016/j.neuron.2006.05.019
- Tirlapur U. K., König K. (2002). Targeted transfection by femtosecond laser. Nature 418, 290 – 291. doi:10.1038/418290a
- Tolić-Nørrelykke I. M., Sacconi L., Thon G., Pavone F. S. (2004). Positioning and elongation of the fission yeast spindle by microtubule-based pushing. Curr. Biol. 14, 1181 – 1186. doi:10.1016/j.cub.2004.06.029
- Trachtenberg J. T., Chen B. E., Knott G. W., Feng G., Sanes J. R., Welker E., Svoboda K. (2002). Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420, 788 – 794. doi:10.1038/nature01273
- Tsai P. S., Blinder P., Migliori B. J., Neev J., Jin Y., Squier J. A., Kleinfeld D. (2009). Plasma-mediated ablation: An optical tool for submicrometer surgery on neuronal and vascular systems. Curr. Opin. Biotechnol. 20, 1 – 10. doi:10.1016/j.copbio.2009.02.003
- Vogel A., Noack J., Hüttman G., Paltauf G. (2005). Mechanisms of femtosecond laser nanosurgery of cells and tissues. Appl. Phys. B 81, 1015 – 1047. doi:10.1007/s00340-005-2036-6
- Vogel A., Venugopalan V. (2003). Mechanisms of pulsed laser ablation of biological tissues. Chem. Rev. 103, 577 – 644. doi:10.1021/cr010379n
- Waller A. (1850). Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 140, 423 – 429. doi:10.1098/rstl.1850.0021
- Watanabe W., Arakawa N. (2004). Femtosecond laser disruption of subcellular organelles in a living cell. Opt. Express 12, 4203 – 4213. doi:10.1364/OPEX.12.004203
- Yanik M. F., Cinar H., Cinar H. N., Chisholm A. D., Jin Y., Ben-Yakar A. (2004). Neurosurgery: functional regeneration after laser axotomy. Nature 432, 822. doi:10.1038/432822a
- Zeira E., Manevitch A., Khatchatouriants A., Pappo O., Hyam E., Darash-Yahana M., Tavor E., Honigman A., Lewis A., Galun E. (2003). Femtosecond infrared laser an efficient and safe in vivo gene delivery system for prolonged expression. Mol. Ther. 8, 342 – 350. doi:10.1016/S1525-0016(03)00184-9
- Zhang S., Boyd J., Delaney K., Murphy T. H. (2005). Rapid reversible changes in dendritic spine structure in vivo gated by the degree of ischemia. J. Neurosci. 25, 5333 – 5338. doi:10.1523/JNEUROSCI.1085-05.2005
- Zhang S., Murphy T. H. (2007). Imaging the impact of cortical microcirculation on synaptic structure and sensory-evoked hemodynamic responses in vivo. PLoS Biol. 5, e119. doi:10.1371/journal.pbio.0050119
- Zimmerman U. P., Schlaepfer W. W. (1984). Multiple forms of Ca-activated protease from rat brain and muscle. J. Biol. Chem. 259, 3210 – 3218.
- Zipfel W. R., Williams R. M., Webb W. W. (2003). Nonlinear magic: multiphoton microscopy in the biosciences. Nat. Biotechnol. 21, 1369 – 1377. doi:10.1038/nbt899
- Zuo Y., Lin A., Chang P., Gan W. B. (2005). Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46, 181 – 189. doi:10.1016/j.neuron.2005.04.001
Citation
Mascaro, A. L. A., et al. (2010). Multi-Photon Nanosurgery in Live Brain. Frontiers in Neuroenergetics, Volume 2. https://doi.org/
- Received
- Accepted
- Published
- Volume
- 2 - 2010
Copyright
Copyright © 2010 Allegra Mascaro, Sacconi and Pavone.
License: http://www.frontiersin.org/licenseagreement
*Correspondence: Francesco S. Pavone
Article metrics
- Views
- 0
- Downloads
- 0
- Citations
- 0
- Shares
- 0
