Optogenetics: Difference between revisions
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'''Optogenetics''' ({{ety|gre| |
'''Optogenetics''' ({{ety|gre|optikós]|seen, visible}}) is a biological technique which involves the use of light to control cells in living tissue, typically [[neurons]], that have been genetically modified to [[gene expression|express]] light-sensitive [[ion channels]]. It is a [[Neuromodulation (medicine)|neuromodulation]] method employed in [[neuroscience]] that uses a combination of techniques from [[optics]] and [[genetics]] to control and monitor the activities of individual [[neuron]]s in [[in vivo|living tissue]]—even within freely-moving animals—and to precisely measure the effects of those manipulations in real-time.<ref name="Deisseroth 2006">{{cite journal|doi=10.1523/JNEUROSCI.3863-06.2006|title=Next-Generation Optical Technologies for Illuminating Genetically Targeted Brain Circuits|year=2006|last1=Deisseroth|first1=K.|last2=Feng|first2=G.|last3=Majewska|first3=A. K.|last4=Miesenbock|first4=G.|last5=Ting|first5=A.|last6=Schnitzer|first6=M. J.|journal=Journal of Neuroscience|volume=26|issue=41|pages=10380–6|pmid=17035522|pmc=2820367}}</ref> The key reagents used in optogenetics are light-sensitive proteins. Neuronal control is achieved using '''optogenetic actuators''' like [[channelrhodopsin]], [[halorhodopsin]], and [[Microbial rhodopsin|archaerhodopsin]], while optical recording of neuronal activities can be made with the help of '''optogenetic sensors''' for calcium ([[GCaMP]]), vesicular release (synaptopHluorin), neurotransmitter (GluSnFRs), or membrane voltage (Arclightning, ASAP1).<ref>{{Cite journal |
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}}</ref> They showed that photostimulation of genetically circumscribed groups of neurons, such as those of the [[dopaminergic]] system, elicited characteristic behavioural changes in fruit flies. In August 2005, [[Karl Deisseroth]]'s laboratory in the Bioengineering Department at Stanford including graduate students [[Edward Boyden|Ed Boyden]] and [[Feng Zhang]] (both now at MIT) published the first demonstration of a single-component optogenetic system, beginning in cultured mammalian neurons.<ref name="Boyden 2005">{{cite journal | last1 = Boyden | first1 = E. S. | last2 = Zhang | first2 = F. | last3 = Bamberg | first3 = E. | last4 = Nagel | first4 = G. | last5 = Deisseroth | first5 = K. | year = 2005 | title = Millisecond-timescale, genetically targeted optical control of neural activity | url = | journal = Nat. Neurosci | volume = 8 | issue = 9| pages = 1263–8 | doi = 10.1038/nn1525 | pmid = 16116447 }}</ref><ref name="Li 2005">{{cite journal|last=Li,|first=X.|author2=Gutierrez, D. V. |author3=Hanson, M. G. |author4=Han, J. |author5=Mark, M. D. |author6=Chiel, H. |author7=Hegemann, P. |author8=Landmesser, L. T. |author9= Herlitze, S. |title=Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin|journal=Proc Natl Acad Sci U S A|date=14 October 2005|volume=102|issue=49|pages=17816–21|url=http://www.pnas.org/content/102/49/17816.full.pdf|bibcode = 2005PNAS..10217816L |doi = 10.1073/pnas.0509030102|pmid=16306259|pmc=1292990}}</ref> using [[Channelrhodopsin-2|channelrhodopsin]], a single-component light-activated [[cation]] channel from unicellular [[algae]], whose molecular identity and principal properties rendering it useful for optogenetic studies had been first reported in November 2003 by Georg Nagel.<ref name="Nagel 2003">{{cite journal|last=Nagel,|first=G.|author2=Szellas, T. |author3=Huhn, W. |author4=Kateriya, S. |author5=Adeishvili, N. |author6=Berthold, P. |author7=Ollig, D. |author8=Hegemann, P. |author9= Bamberg, E. |title=Channelrhodopsin-2, a directly light-gated cation-selective membrane channel|journal=Proc Natl Acad Sci U S A|date=25 November 2003|volume=100|issue=24|pages=13940–5|doi=10.1073/pnas.1936192100|bibcode = 2003PNAS..10013940N|pmc=283525|pmid=14615590}}</ref> The groups of Gottschalk and Nagel were the first to extend the usability of Channelrhodopsin-2 for controlling neuronal activity to the intact animal by showing that motor patterns in the roundworm ''[[Caenorhabditis elegans]]'' could be evoked by targeted expression and stimulation of Channelrhodopsin-2 in selected neural circuits (published in December 2005).<ref>{{cite journal |author1=Nagel, G. |author2=Brauner, M. |author3=Liewald, J. F. |author4=Adeishvili, N. |author5=Bamberg, E. |author6=Gottschalk, A. |title=Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses |journal=Curr. Biol. |volume=15 |issue=24 |pages=2279–84 |date=December 2005 |pmid=16360690 |doi=10.1016/j.cub.2005.11.032 }}</ref> Now optogenetics has been routinely combined with brain region-and cell type-specific Cre/loxP genetic methods developed for Neuroscience by [[Joe Z. Tsien]] back in 1990s <ref>{{cite journal | last1 = Tsien | first1 = JZ | display-authors = etal | date = Dec 1996 | title = Subregion- and cell type-restricted gene knockout in mouse brain | url = http://www.sciencedirect.com/science/article/pii/S0092867400818267 | journal = Cell. | volume = 87 | issue = 7| pages = 1317–26 | doi=10.1016/S0092-8674(00)81826-7}}</ref> to activate or inhibit specific brain regions and cell-types in vivo.<ref name="pmid26925095">Tsien JZ (2016) [https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&retmode=ref&cmd=prlinks&id=26925095 Cre-Lox Neurogenetics: 20 Years of Versatile Applications in Brain Research and Counting….] ''Front Genet'' 7 ():19. |
}}</ref> They showed that photostimulation of genetically circumscribed groups of neurons, such as those of the [[dopaminergic]] system, elicited characteristic behavioural changes in fruit flies. In August 2005, [[Karl Deisseroth]]'s laboratory in the Bioengineering Department at Stanford including graduate students [[Edward Boyden|Ed Boyden]] and [[Feng Zhang]] (both now at MIT) published the first demonstration of a single-component optogenetic system, beginning in cultured mammalian neurons.<ref name="Boyden 2005">{{cite journal | last1 = Boyden | first1 = E. S. | last2 = Zhang | first2 = F. | last3 = Bamberg | first3 = E. | last4 = Nagel | first4 = G. | last5 = Deisseroth | first5 = K. | year = 2005 | title = Millisecond-timescale, genetically targeted optical control of neural activity | url = | journal = Nat. Neurosci | volume = 8 | issue = 9| pages = 1263–8 | doi = 10.1038/nn1525 | pmid = 16116447 }}</ref><ref name="Li 2005">{{cite journal|last=Li,|first=X.|author2=Gutierrez, D. V. |author3=Hanson, M. G. |author4=Han, J. |author5=Mark, M. D. |author6=Chiel, H. |author7=Hegemann, P. |author8=Landmesser, L. T. |author9= Herlitze, S. |title=Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin|journal=Proc Natl Acad Sci U S A|date=14 October 2005|volume=102|issue=49|pages=17816–21|url=http://www.pnas.org/content/102/49/17816.full.pdf|bibcode = 2005PNAS..10217816L |doi = 10.1073/pnas.0509030102|pmid=16306259|pmc=1292990}}</ref> using [[Channelrhodopsin-2|channelrhodopsin]], a single-component light-activated [[cation]] channel from unicellular [[algae]], whose molecular identity and principal properties rendering it useful for optogenetic studies had been first reported in November 2003 by Georg Nagel.<ref name="Nagel 2003">{{cite journal|last=Nagel,|first=G.|author2=Szellas, T. |author3=Huhn, W. |author4=Kateriya, S. |author5=Adeishvili, N. |author6=Berthold, P. |author7=Ollig, D. |author8=Hegemann, P. |author9= Bamberg, E. |title=Channelrhodopsin-2, a directly light-gated cation-selective membrane channel|journal=Proc Natl Acad Sci U S A|date=25 November 2003|volume=100|issue=24|pages=13940–5|doi=10.1073/pnas.1936192100|bibcode = 2003PNAS..10013940N|pmc=283525|pmid=14615590}}</ref> The groups of Gottschalk and Nagel were the first to extend the usability of Channelrhodopsin-2 for controlling neuronal activity to the intact animal by showing that motor patterns in the roundworm ''[[Caenorhabditis elegans]]'' could be evoked by targeted expression and stimulation of Channelrhodopsin-2 in selected neural circuits (published in December 2005).<ref>{{cite journal |author1=Nagel, G. |author2=Brauner, M. |author3=Liewald, J. F. |author4=Adeishvili, N. |author5=Bamberg, E. |author6=Gottschalk, A. |title=Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses |journal=Curr. Biol. |volume=15 |issue=24 |pages=2279–84 |date=December 2005 |pmid=16360690 |doi=10.1016/j.cub.2005.11.032 }}</ref> Now optogenetics has been routinely combined with brain region-and cell type-specific Cre/loxP genetic methods developed for Neuroscience by [[Joe Z. Tsien]] back in 1990s <ref>{{cite journal | last1 = Tsien | first1 = JZ | display-authors = etal | date = Dec 1996 | title = Subregion- and cell type-restricted gene knockout in mouse brain | url = http://www.sciencedirect.com/science/article/pii/S0092867400818267 | journal = Cell. | volume = 87 | issue = 7| pages = 1317–26 | doi=10.1016/S0092-8674(00)81826-7}}</ref> to activate or inhibit specific brain regions and cell-types in vivo.<ref name="pmid26925095">Tsien JZ (2016) [https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&retmode=ref&cmd=prlinks&id=26925095 Cre-Lox Neurogenetics: 20 Years of Versatile Applications in Brain Research and Counting….] ''Front Genet'' 7 ():19. {{DOI|10.3389/fgene.2016.00019}} PMID 26925095</ref> |
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The primary tools for optogenetic recordings have been genetically encoded calcium indicators (GECIs). The first GECI to be used to image activity in an animal was [[Cameleon (protein)|cameleon]], designed by Atsushi Miyawaki, [[Roger Y. Tsien|Roger Tsien]] and coworkers.<ref>{{Cite journal|title = Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin|url = http://www.ncbi.nlm.nih.gov/pubmed/9278050|journal = Nature|date = 1997-08-28|issn = 0028-0836|pmid = 9278050|pages = 882–887|volume = 388|issue = 6645|doi = 10.1038/42264|first = A.|last = Miyawaki|first2 = J.|last2 = Llopis|first3 = R.|last3 = Heim|first4 = J. M.|last4 = McCaffery|first5 = J. A.|last5 = Adams|first6 = M.|last6 = Ikura|first7 = R. Y.|last7 = Tsien}}</ref> Cameleon was first used successfully in an animal by Rex Kerr, William Schafer and coworkers to record from neurons and muscle cells of the nematode ''[[Caenorhabditis elegans|C. elegans]]''.<ref>{{Cite journal|title = Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans|url = http://www.ncbi.nlm.nih.gov/pubmed/10896155|journal = Neuron|date = 2000-06-01|issn = 0896-6273|pmid = 10896155|pages = 583–594|volume = 26|issue = 3|first = R.|last = Kerr|first2 = V.|last2 = Lev-Ram|first3 = G.|last3 = Baird|first4 = P.|last4 = Vincent|first5 = R. Y.|last5 = Tsien|first6 = W. R.|last6 = Schafer|doi=10.1016/s0896-6273(00)81196-4}}</ref> Cameleon was subsequently used to record neural activity in flies<ref>{{Cite journal|title = Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons|url = http://www.ncbi.nlm.nih.gov/pubmed/12419190|journal = Current Biology|date = 2002-10-29|issn = 0960-9822|pmid = 12419190|pages = 1877–1884|volume = 12|issue = 21|first = André|last = Fiala|first2 = Thomas|last2 = Spall|first3 = Sören|last3 = Diegelmann|first4 = Beate|last4 = Eisermann|first5 = Silke|last5 = Sachse|first6 = Jean-Marc|last6 = Devaud|first7 = Erich|last7 = Buchner|first8 = C. Giovanni|last8 = Galizia|doi=10.1016/s0960-9822(02)01239-3}}</ref> and zebrafish.<ref>{{Cite journal|title = Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator|url = http://www.ncbi.nlm.nih.gov/pubmed/12930818|journal = Journal of Neurophysiology|date = 2003-12-01|issn = 0022-3077|pmid = 12930818|pages = 3986–3997|volume = 90|issue = 6|doi = 10.1152/jn.00576.2003|first = Shin-ichi|last = Higashijima|first2 = Mark A.|last2 = Masino|first3 = Gail|last3 = Mandel|first4 = Joseph R.|last4 = Fetcho}}</ref> In mammals, the first GECI to be used in vivo was [[GCaMP]],<ref>{{Cite journal|title = Ca2+-sensing transgenic mice: postsynaptic signaling in smooth muscle|url = http://www.ncbi.nlm.nih.gov/pubmed/14990564|journal = The Journal of Biological Chemistry|date = 2004-05-14|issn = 0021-9258|pmid = 14990564|pages = 21461–21468|volume = 279|issue = 20|doi = 10.1074/jbc.M401084200|first = Guangju|last = Ji|first2 = Morris E.|last2 = Feldman|first3 = Ke-Yu|last3 = Deng|first4 = Kai Su|last4 = Greene|first5 = Jason|last5 = Wilson|first6 = Jane C.|last6 = Lee|first7 = Robyn C.|last7 = Johnston|first8 = Mark|last8 = Rishniw|first9 = Yvonne|last9 = Tallini}}</ref> first developed by Nakai and coworkers.<ref>{{Cite journal|title = A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein|url = http://www.ncbi.nlm.nih.gov/pubmed/11175727|journal = Nature Biotechnology|date = 2001-02-01|issn = 1087-0156|pmid = 11175727|pages = 137–141|volume = 19|issue = 2|doi = 10.1038/84397|first = J.|last = Nakai|first2 = M.|last2 = Ohkura|first3 = K.|last3 = Imoto}}</ref> GCaMP has undergone numerous improvements, and GCaMP6<ref>{{Cite journal|title = Ultrasensitive fluorescent proteins for imaging neuronal activity|journal = Nature|date = 2013-07-18|issn = 1476-4687|pmc = 3777791|pmid = 23868258|pages = 295–300|volume = 499|issue = 7458|doi = 10.1038/nature12354|first = Tsai-Wen|last = Chen|first2 = Trevor J.|last2 = Wardill|first3 = Yi|last3 = Sun|first4 = Stefan R.|last4 = Pulver|first5 = Sabine L.|last5 = Renninger|first6 = Amy|last6 = Baohan|first7 = Eric R.|last7 = Schreiter|first8 = Rex A.|last8 = Kerr|first9 = Michael B.|last9 = Orger}}</ref> in particular has become widely used throughout neuroscience. |
The primary tools for optogenetic recordings have been genetically encoded calcium indicators (GECIs). The first GECI to be used to image activity in an animal was [[Cameleon (protein)|cameleon]], designed by Atsushi Miyawaki, [[Roger Y. Tsien|Roger Tsien]] and coworkers.<ref>{{Cite journal|title = Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin|url = http://www.ncbi.nlm.nih.gov/pubmed/9278050|journal = Nature|date = 1997-08-28|issn = 0028-0836|pmid = 9278050|pages = 882–887|volume = 388|issue = 6645|doi = 10.1038/42264|first = A.|last = Miyawaki|first2 = J.|last2 = Llopis|first3 = R.|last3 = Heim|first4 = J. M.|last4 = McCaffery|first5 = J. A.|last5 = Adams|first6 = M.|last6 = Ikura|first7 = R. Y.|last7 = Tsien}}</ref> Cameleon was first used successfully in an animal by Rex Kerr, William Schafer and coworkers to record from neurons and muscle cells of the nematode ''[[Caenorhabditis elegans|C. elegans]]''.<ref>{{Cite journal|title = Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans|url = http://www.ncbi.nlm.nih.gov/pubmed/10896155|journal = Neuron|date = 2000-06-01|issn = 0896-6273|pmid = 10896155|pages = 583–594|volume = 26|issue = 3|first = R.|last = Kerr|first2 = V.|last2 = Lev-Ram|first3 = G.|last3 = Baird|first4 = P.|last4 = Vincent|first5 = R. Y.|last5 = Tsien|first6 = W. R.|last6 = Schafer|doi=10.1016/s0896-6273(00)81196-4}}</ref> Cameleon was subsequently used to record neural activity in flies<ref>{{Cite journal|title = Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons|url = http://www.ncbi.nlm.nih.gov/pubmed/12419190|journal = Current Biology|date = 2002-10-29|issn = 0960-9822|pmid = 12419190|pages = 1877–1884|volume = 12|issue = 21|first = André|last = Fiala|first2 = Thomas|last2 = Spall|first3 = Sören|last3 = Diegelmann|first4 = Beate|last4 = Eisermann|first5 = Silke|last5 = Sachse|first6 = Jean-Marc|last6 = Devaud|first7 = Erich|last7 = Buchner|first8 = C. Giovanni|last8 = Galizia|doi=10.1016/s0960-9822(02)01239-3}}</ref> and zebrafish.<ref>{{Cite journal|title = Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator|url = http://www.ncbi.nlm.nih.gov/pubmed/12930818|journal = Journal of Neurophysiology|date = 2003-12-01|issn = 0022-3077|pmid = 12930818|pages = 3986–3997|volume = 90|issue = 6|doi = 10.1152/jn.00576.2003|first = Shin-ichi|last = Higashijima|first2 = Mark A.|last2 = Masino|first3 = Gail|last3 = Mandel|first4 = Joseph R.|last4 = Fetcho}}</ref> In mammals, the first GECI to be used in vivo was [[GCaMP]],<ref>{{Cite journal|title = Ca2+-sensing transgenic mice: postsynaptic signaling in smooth muscle|url = http://www.ncbi.nlm.nih.gov/pubmed/14990564|journal = The Journal of Biological Chemistry|date = 2004-05-14|issn = 0021-9258|pmid = 14990564|pages = 21461–21468|volume = 279|issue = 20|doi = 10.1074/jbc.M401084200|first = Guangju|last = Ji|first2 = Morris E.|last2 = Feldman|first3 = Ke-Yu|last3 = Deng|first4 = Kai Su|last4 = Greene|first5 = Jason|last5 = Wilson|first6 = Jane C.|last6 = Lee|first7 = Robyn C.|last7 = Johnston|first8 = Mark|last8 = Rishniw|first9 = Yvonne|last9 = Tallini}}</ref> first developed by Nakai and coworkers.<ref>{{Cite journal|title = A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein|url = http://www.ncbi.nlm.nih.gov/pubmed/11175727|journal = Nature Biotechnology|date = 2001-02-01|issn = 1087-0156|pmid = 11175727|pages = 137–141|volume = 19|issue = 2|doi = 10.1038/84397|first = J.|last = Nakai|first2 = M.|last2 = Ohkura|first3 = K.|last3 = Imoto}}</ref> GCaMP has undergone numerous improvements, and GCaMP6<ref>{{Cite journal|title = Ultrasensitive fluorescent proteins for imaging neuronal activity|journal = Nature|date = 2013-07-18|issn = 1476-4687|pmc = 3777791|pmid = 23868258|pages = 295–300|volume = 499|issue = 7458|doi = 10.1038/nature12354|first = Tsai-Wen|last = Chen|first2 = Trevor J.|last2 = Wardill|first3 = Yi|last3 = Sun|first4 = Stefan R.|last4 = Pulver|first5 = Sabine L.|last5 = Renninger|first6 = Amy|last6 = Baohan|first7 = Eric R.|last7 = Schreiter|first8 = Rex A.|last8 = Kerr|first9 = Michael B.|last9 = Orger}}</ref> in particular has become widely used throughout neuroscience. |
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Millisecond-scale temporal precision is central to optogenetics, which allows the experimenter to keep pace with fast biological information processing (for example, in probing the causal role of specific [[action potential]] patterns in defined neurons). Indeed, to probe the neural code, optogenetics by definition must operate on the millisecond timescale to allow addition or deletion of precise activity patterns within specific cells in the brains of intact animals, including mammals (see '''Figure 1)'''. By comparison, the temporal precision of traditional genetic manipulations (employed to probe the causal role of specific genes within cells, via "loss-of-function" or "gain of function" changes in these genes) is rather slow, from hours or days to months. It is important to also have fast readouts in optogenetics that can keep pace with the optical control. This can be done with electrical recordings ("optrodes") or with reporter proteins that are [[biosensor]]s, where scientists have fused fluorescent proteins to detector proteins. An example of this is [[Voltage-sensitive protein|voltage-sensitive fluorescent protein]] (VSFP2).<ref name="pmid22815406">Akemann W, Mutoh H, Perron A, Park YK, Iwamoto Y, Knöpfel T (2012) [https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&retmode=ref&cmd=prlinks&id=22815406 Imaging neural circuit dynamics with a voltage-sensitive fluorescent protein.] ''J Neurophysiol'' 108 (8):2323-37. |
Millisecond-scale temporal precision is central to optogenetics, which allows the experimenter to keep pace with fast biological information processing (for example, in probing the causal role of specific [[action potential]] patterns in defined neurons). Indeed, to probe the neural code, optogenetics by definition must operate on the millisecond timescale to allow addition or deletion of precise activity patterns within specific cells in the brains of intact animals, including mammals (see '''Figure 1)'''. By comparison, the temporal precision of traditional genetic manipulations (employed to probe the causal role of specific genes within cells, via "loss-of-function" or "gain of function" changes in these genes) is rather slow, from hours or days to months. It is important to also have fast readouts in optogenetics that can keep pace with the optical control. This can be done with electrical recordings ("optrodes") or with reporter proteins that are [[biosensor]]s, where scientists have fused fluorescent proteins to detector proteins. An example of this is [[Voltage-sensitive protein|voltage-sensitive fluorescent protein]] (VSFP2).<ref name="pmid22815406">Akemann W, Mutoh H, Perron A, Park YK, Iwamoto Y, Knöpfel T (2012) [https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&retmode=ref&cmd=prlinks&id=22815406 Imaging neural circuit dynamics with a voltage-sensitive fluorescent protein.] ''J Neurophysiol'' 108 (8):2323-37. {{DOI|10.1152/jn.00452.2012}} PMID 22815406 </ref> |
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The hallmark of optogenetics therefore is introduction of fast light-activated channels and enzymes that allow temporally precise manipulation of electrical and biochemical events while maintaining cell-type resolution through the use of specific targeting mechanisms. Among the microbial opsins which can be used to investigate the function of neural systems are the [[channelrhodopsin]]s (ChR2, ChR1, VChR1, and SFOs) to excite neurons. For silencing, [[halorhodopsin]] (NpHR),<ref name="Zhao 2008">{{Cite journal |
The hallmark of optogenetics therefore is introduction of fast light-activated channels and enzymes that allow temporally precise manipulation of electrical and biochemical events while maintaining cell-type resolution through the use of specific targeting mechanisms. Among the microbial opsins which can be used to investigate the function of neural systems are the [[channelrhodopsin]]s (ChR2, ChR1, VChR1, and SFOs) to excite neurons. For silencing, [[halorhodopsin]] (NpHR),<ref name="Zhao 2008">{{Cite journal |
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}}</ref> [[archaerhodopsin]] (Arch), [[Leptosphaeria maculans]] fungal opsins (Mac), and enhanced bacteriorhodopsin (eBR) have been employed to inhibit neurons (see '''Figure 2'''), including in freely-moving mammals.<ref name="Witten 2010">{{cite journal | last1 = Witten | first1 = I. B. | last2 = Lin | first2 = S. C. | last3 = Brodsky | first3 = M. | last4 = Prakash | first4 = R. | last5 = Diester | first5 = I. | last6 = Anikeeva | first6 = P. | last7 = Gradinaru | first7 = V. | last8 = Ramakrishnan | first8 = C. | last9 = Deisseroth | first9 = K. | year = 2010 | title = Cholinergic interneurons control local circuit activity and cocaine conditioning | url = | journal = Science | volume = 330 | issue = 6011| pages = 1677–81 | doi = 10.1126/science.1193771 | pmid = 21164015 | pmc=3142356}}</ref> |
}}</ref> [[archaerhodopsin]] (Arch), [[Leptosphaeria maculans]] fungal opsins (Mac), and enhanced bacteriorhodopsin (eBR) have been employed to inhibit neurons (see '''Figure 2'''), including in freely-moving mammals.<ref name="Witten 2010">{{cite journal | last1 = Witten | first1 = I. B. | last2 = Lin | first2 = S. C. | last3 = Brodsky | first3 = M. | last4 = Prakash | first4 = R. | last5 = Diester | first5 = I. | last6 = Anikeeva | first6 = P. | last7 = Gradinaru | first7 = V. | last8 = Ramakrishnan | first8 = C. | last9 = Deisseroth | first9 = K. | year = 2010 | title = Cholinergic interneurons control local circuit activity and cocaine conditioning | url = | journal = Science | volume = 330 | issue = 6011| pages = 1677–81 | doi = 10.1126/science.1193771 | pmid = 21164015 | pmc=3142356}}</ref> |
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Moreover, optogenetic control of well-defined biochemical events within behaving mammals is now also possible. Building on prior work fusing vertebrate [[opsins]] to specific [[G-protein coupled receptors]] <ref>{{cite journal | last1 = Kim | first1 = J. M. | last2 = Hwa | first2 = J. | last3 = Garriga | first3 = P. | last4 = Reeves | first4 = P. J. | last5 = RajBhandary | first5 = U. L. | last6 = Khorana | first6 = H. G. | year = 2005 | title = Light-driven activation of beta 2-adrenergic receptor signaling by a chimeric rhodopsin containing the beta 2-adrenergic receptor cytoplasmic loops | url = | journal = Biochemistry | volume = 44 | issue = 7| pages = 2284–92 | doi = 10.1021/bi048328i | pmid = 15709741 }}</ref> a family of [[chimera (genetics)|chimeric]] single-component optogenetic tools was created that allowed researchers to manipulate within behaving mammals the concentration of defined intracellular messengers such as cAMP and IP3 in targeted cells <ref name="Airan 2009">{{cite journal | last1 = Airan | first1 = R. D. | last2 = Thompson | first2 = K. R. | last3 = Fenno | first3 = L. E. | last4 = Bernstein | first4 = H. | last5 = Deisseroth | first5 = K. | year = 2009 | title = Temporally precise in vivo control of intracellular signalling | url = | journal = Nature | volume = 458 | issue = 7241| pages = 1025–9 | doi = 10.1038/nature07926 | pmid = 19295515 |bibcode = 2009Natur.458.1025A }}</ref> Other biochemical approaches to optogenetics (crucially, with tools that displayed low activity in the dark) followed soon thereafter, when optical control over small GTPases and adenylyl cyclases was achieved in cultured cells using novel strategies from several different laboratories.<ref>{{cite journal | doi = 10.1038/nature08446 | pmid = 19749742 | pmc=2989900 | volume=461 | issue=7266 | title=Spatiotemporal control of cell signalling using a light-switchable protein interaction |date=October 2009 | journal=Nature | pages=997–1001|bibcode = 2009Natur.461..997L | last1 = Levskaya | first1 = Anselm | last2 = Weiner | first2 = Orion D. | last3 = Lim | first3 = Wendell A. | last4 = Voigt | first4 = Christopher A. }}</ref><ref>{{cite journal | doi = 10.1038/nature08241 | pmid = 19693014 | pmc=2766670 | volume=461 | issue=7260 | title=A genetically encoded photoactivatable Rac controls the motility of living cells |date=September 2009 | journal=Nature | pages=104–8|bibcode = 2009Natur.461..104W | last1 = Wu | first1 = Yi I. | last2 = Frey | first2 = Daniel | last3 = Lungu | first3 = Oana I. | last4 = Jaehrig | first4 = Angelika | last5 = Schlichting | first5 = Ilme |authorlink5=Ilme Schlichting | last6 = Kuhlman | first6 = Brian | last7 = Hahn | first7 = Klaus M. |
Moreover, optogenetic control of well-defined biochemical events within behaving mammals is now also possible. Building on prior work fusing vertebrate [[opsins]] to specific [[G-protein coupled receptors]] <ref>{{cite journal | last1 = Kim | first1 = J. M. | last2 = Hwa | first2 = J. | last3 = Garriga | first3 = P. | last4 = Reeves | first4 = P. J. | last5 = RajBhandary | first5 = U. L. | last6 = Khorana | first6 = H. G. | year = 2005 | title = Light-driven activation of beta 2-adrenergic receptor signaling by a chimeric rhodopsin containing the beta 2-adrenergic receptor cytoplasmic loops | url = | journal = Biochemistry | volume = 44 | issue = 7| pages = 2284–92 | doi = 10.1021/bi048328i | pmid = 15709741 }}</ref> a family of [[chimera (genetics)|chimeric]] single-component optogenetic tools was created that allowed researchers to manipulate within behaving mammals the concentration of defined intracellular messengers such as cAMP and IP3 in targeted cells <ref name="Airan 2009">{{cite journal | last1 = Airan | first1 = R. D. | last2 = Thompson | first2 = K. R. | last3 = Fenno | first3 = L. E. | last4 = Bernstein | first4 = H. | last5 = Deisseroth | first5 = K. | year = 2009 | title = Temporally precise in vivo control of intracellular signalling | url = | journal = Nature | volume = 458 | issue = 7241| pages = 1025–9 | doi = 10.1038/nature07926 | pmid = 19295515 |bibcode = 2009Natur.458.1025A }}</ref> Other biochemical approaches to optogenetics (crucially, with tools that displayed low activity in the dark) followed soon thereafter, when optical control over small GTPases and adenylyl cyclases was achieved in cultured cells using novel strategies from several different laboratories.<ref>{{cite journal | doi = 10.1038/nature08446 | pmid = 19749742 | pmc=2989900 | volume=461 | issue=7266 | title=Spatiotemporal control of cell signalling using a light-switchable protein interaction |date=October 2009 | journal=Nature | pages=997–1001|bibcode = 2009Natur.461..997L | last1 = Levskaya | first1 = Anselm | last2 = Weiner | first2 = Orion D. | last3 = Lim | first3 = Wendell A. | last4 = Voigt | first4 = Christopher A. }}</ref><ref>{{cite journal | doi = 10.1038/nature08241 | pmid = 19693014 | pmc=2766670 | volume=461 | issue=7260 | title=A genetically encoded photoactivatable Rac controls the motility of living cells |date=September 2009 | journal=Nature | pages=104–8|bibcode = 2009Natur.461..104W | last1 = Wu | first1 = Yi I. | last2 = Frey | first2 = Daniel | last3 = Lungu | first3 = Oana I. | last4 = Jaehrig | first4 = Angelika | last5 = Schlichting | first5 = Ilme |authorlink5=Ilme Schlichting | last6 = Kuhlman | first6 = Brian | last7 = Hahn | first7 = Klaus M. |pmc=2766670 |pmid=19693014}}</ref><ref>{{cite journal | last1 = Yazawa | first1 = M. | last2 = Sadaghiani | first2 = A. M. | last3 = Hsueh | first3 = B. | last4 = Dolmetsch | first4 = R. E. | year = 2009 | title = Induction of protein-protein interactions in live cells using light | url = | journal = Nature Biotechnology | volume = 27 | issue = 10| pages = 941–5 | doi = 10.1038/nbt.1569 | pmid = 19801976 }}</ref><ref>{{cite journal | doi = 10.1074/jbc.M110.185496 | pmid = 21030594 | pmc=3020725 | volume=286 | issue=2 | title=Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium Beggiatoa |date=January 2011 | journal=J. Biol. Chem. | pages=1181–8 | last1 = Stierl | first1 = M. | last2 = Stumpf | first2 = P. | last3 = Udwari | first3 = D. | last4 = Gueta | first4 = R. | last5 = Hagedorn | first5 = R. | last6 = Losi | first6 = A. | last7 = Gartner | first7 = W. | last8 = Petereit | first8 = L. | last9 = Efetova | first9 = M.| last10 = Schwarzel | first10 = M. | last11 = Oertner | first11 = T. G. | last12 = Nagel | first12 = G. | last13 = Hegemann | first13 = P. | display-authors = 8 }}</ref><ref>{{cite journal | doi = 10.1074/jbc.M110.177600 | pmid = 21030591 | pmc=3009876 | volume=285 | issue=53 | title=Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications |date=December 2010 | journal=J. Biol. Chem. | pages=41501–8 | last1 = Ryu | first1 = M.-H. | last2 = Moskvin | first2 = O. V. | last3 = Siltberg-Liberles | first3 = J. | last4 = Gomelsky | first4 = M.}}</ref> This emerging repertoire of optogenetic probes now allows cell-type-specific and temporally precise control of multiple axes of cellular function within intact animals.<ref name="pmid26967281">Lerner TN, Ye L, Deisseroth K (2016) [https://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&retmode=ref&cmd=prlinks&id=26967281 Communication in Neural Circuits: Tools, Opportunities, and Challenges.] ''Cell'' 164 (6):1136-50. {{DOI|10.1016/j.cell.2016.02.027}} PMID 26967281</ref> |
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Optogenetics also necessarily includes 1) the development of genetic targeting strategies such as cell-specific promoters or other customized conditionally-active viruses, to deliver the light-sensitive probes to specific populations of neurons in the brain of living animals (e.g. worms, fruit flies, mice, rats, and monkeys), and 2) hardware (e.g. integrated fiberoptic and solid-state light sources) to allow specific cell types, even deep within the brain, to be controlled in freely behaving animals. Most commonly, the latter is now achieved using the fiberoptic-coupled diode technology introduced in 2007,<ref name="Aravanis 2007">{{cite journal | doi = 10.1088/1741-2560/4/3/S02 | pmid = 17873414 | volume=4 | issue=3 | title=An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology |date=September 2007 | journal=J Neural Eng | pages=S143–56|bibcode = 2007JNEng...4S.143A | last1 = Aravanis | first1 = Alexander M | last2 = Wang | first2 = Li-Ping | last3 = Zhang | first3 = Feng | last4 = Meltzer | first4 = Leslie A | last5 = Mogri | first5 = Murtaza Z | last6 = Schneider | first6 = M Bret | last7 = Deisseroth | first7 = Karl }}. PMID 17873414</ref><ref name="Adamantidis 2007">{{cite journal | doi = 10.1038/nature06310 | pmid = 17943086 | volume=450 | issue=7168 | title=Neural substrates of awakening probed with optogenetic control of hypocretin neurons |date=November 2007 | journal=Nature | pages=420–4|bibcode = 2007Natur.450..420A | last1 = Adamantidis | first1 = Antoine R. | last2 = Zhang | first2 = Feng | last3 = Aravanis | first3 = Alexander M. | last4 = Deisseroth | first4 = Karl | last5 = De Lecea | first5 = Luis |
Optogenetics also necessarily includes 1) the development of genetic targeting strategies such as cell-specific promoters or other customized conditionally-active viruses, to deliver the light-sensitive probes to specific populations of neurons in the brain of living animals (e.g. worms, fruit flies, mice, rats, and monkeys), and 2) hardware (e.g. integrated fiberoptic and solid-state light sources) to allow specific cell types, even deep within the brain, to be controlled in freely behaving animals. Most commonly, the latter is now achieved using the fiberoptic-coupled diode technology introduced in 2007,<ref name="Aravanis 2007">{{cite journal | doi = 10.1088/1741-2560/4/3/S02 | pmid = 17873414 | volume=4 | issue=3 | title=An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology |date=September 2007 | journal=J Neural Eng | pages=S143–56|bibcode = 2007JNEng...4S.143A | last1 = Aravanis | first1 = Alexander M | last2 = Wang | first2 = Li-Ping | last3 = Zhang | first3 = Feng | last4 = Meltzer | first4 = Leslie A | last5 = Mogri | first5 = Murtaza Z | last6 = Schneider | first6 = M Bret | last7 = Deisseroth | first7 = Karl }}. PMID 17873414</ref><ref name="Adamantidis 2007">{{cite journal | doi = 10.1038/nature06310 | pmid = 17943086 | volume=450 | issue=7168 | title=Neural substrates of awakening probed with optogenetic control of hypocretin neurons |date=November 2007 | journal=Nature | pages=420–4|bibcode = 2007Natur.450..420A | last1 = Adamantidis | first1 = Antoine R. | last2 = Zhang | first2 = Feng | last3 = Aravanis | first3 = Alexander M. | last4 = Deisseroth | first4 = Karl | last5 = De Lecea | first5 = Luis |pmid=17943086</ref><ref name="Gradinaru 2007">{{cite journal | last1 = Gradinaru | first1 = V. | last2 = Thompson | first2 = K. R. | last3 = Zhang | first3 = F. | last4 = Mogri | first4 = M. | year = 2007| title = Targeting and readout strategies for fast optical neural control in vitro and in vivo | url = | journal = J. Neurosci | volume = 27 | issue = 52| pages = 14231–8 | doi = 10.1523/JNEUROSCI.3578-07.2007 | pmid = 18160630 | last5 = Kay | first5 = K. | last6 = Schneider | first6 = M. B. | last7 = Deisseroth | first7 = K. }}</ref> though to avoid use of implanted electrodes, researchers have engineered ways to inscribe a "window" made of zirconia that has been modified to be transparent and implanted in mice skulls, to allow optical waves to penetrate more deeply to stimulate or inhibit individual neurons.<ref name=Nanomedicine201308>{{cite journal |last1=Damestani |first1= Yasaman |last2= Reynolds|first2= Carissa L.|last3= Szu |first3= Jenny |last4= Hsu |first4= Mike S. |last5= Kodera |first5= Yasuhiro |last6= Binder |first6= Devin K. |last7= Park |first7= B. Hyle |last8= Garay |first8= Javier E. |last9= Rao |first9= Masaru P. |last10= Aguilar |first10= Guillermo |year=2013 |title=Transparent nanocrystalline yttria-stabilized-zirconia calvarium prosthesis |journal=Nanomedicine |volume= 9|issue= 8|pages= 1135–8|publisher=Elsevier Inc. |doi=10.1016/j.nano.2013.08.002 |pmid= 23969102 |url=http://www.nanomedjournal.com/article/S1549-9634(13)00361-4/abstract |accessdate=September 11, 2013}} • Explained by {{cite web |url=http://www.latimes.com/science/sciencenow/la-sci-sn-window-brain-20130903,0,6788242.story |title=A window to the brain? It's here, says UC Riverside team |last=Mohan |first=Geoffrey |date=September 4, 2013 |website=Los Angeles Times |archiveurl= |archivedate= }}</ref> |
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To stimulate superficial brain areas such as the cerebral cortex, optical fibers or [[LED]]s can be directly mounted to the skull of the animal. More deeply implanted optical fibers have been used to deliver light to deeper brain areas. Complementary to fiber-tethered approaches, completely wireless techniques have been developed utilizing wirelessly delivered power to headborne LEDs for unhindered study of complex behaviors in freely behaving vertebrates.<ref name="Wentz 2011">{{cite journal | doi = 10.1088/1741-2560/8/4/046021 | pmid = 21701058 | title = A wirelessly powered and controlled device for optical neural control of freely-behaving animals | year = 2011 | last1 = Wentz | first1 = Christian T | last2 = Bernstein | first2 = Jacob G | last3 = Monahan | first3 = Patrick | last4 = Guerra | first4 = Alexander | last5 = Rodriguez | first5 = Alex | last6 = Boyden | first6 = Edward S | journal = Journal of Neural Engineering | volume = 8 | issue = 4 | pages = 046021 | pmc = 3151576 |bibcode = 2011JNEng...8d6021W }}</ref> In invertebrates such as worms and fruit flies some amount of [[retinal isomerase]] all-trans-retinal (ATR) is supplemented with food. A key advantage of microbial opsins as noted above is that they are fully functional without the addition of exogenous co-factors in vertebrates. |
To stimulate superficial brain areas such as the cerebral cortex, optical fibers or [[LED]]s can be directly mounted to the skull of the animal. More deeply implanted optical fibers have been used to deliver light to deeper brain areas. Complementary to fiber-tethered approaches, completely wireless techniques have been developed utilizing wirelessly delivered power to headborne LEDs for unhindered study of complex behaviors in freely behaving vertebrates.<ref name="Wentz 2011">{{cite journal | doi = 10.1088/1741-2560/8/4/046021 | pmid = 21701058 | title = A wirelessly powered and controlled device for optical neural control of freely-behaving animals | year = 2011 | last1 = Wentz | first1 = Christian T | last2 = Bernstein | first2 = Jacob G | last3 = Monahan | first3 = Patrick | last4 = Guerra | first4 = Alexander | last5 = Rodriguez | first5 = Alex | last6 = Boyden | first6 = Edward S | journal = Journal of Neural Engineering | volume = 8 | issue = 4 | pages = 046021 | pmc = 3151576 |bibcode = 2011JNEng...8d6021W }}</ref> In invertebrates such as worms and fruit flies some amount of [[retinal isomerase]] all-trans-retinal (ATR) is supplemented with food. A key advantage of microbial opsins as noted above is that they are fully functional without the addition of exogenous co-factors in vertebrates. |
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*{{cite journal |author1=Airan, R. D. |author2=Hu, E. S. |author3=Vijaykumar, R. |author4=Roy, M. |author5=Meltzer, L. A. |author6=Deisseroth, K. |title=Integration of light-controlled neuronal firing and fast circuit imaging |journal=Current Opinion in Neurobiology |volume=17 |issue=5 |pages=587–92 |date=October 2007 |pmid=18093822 |doi=10.1016/j.conb.2007.11.003 |url=http://linkinghub.elsevier.com/retrieve/pii/S0959-4388(07)00121-3|ref=refAiran2007}} |
*{{cite journal |author1=Airan, R. D. |author2=Hu, E. S. |author3=Vijaykumar, R. |author4=Roy, M. |author5=Meltzer, L. A. |author6=Deisseroth, K. |title=Integration of light-controlled neuronal firing and fast circuit imaging |journal=Current Opinion in Neurobiology |volume=17 |issue=5 |pages=587–92 |date=October 2007 |pmid=18093822 |doi=10.1016/j.conb.2007.11.003 |url=http://linkinghub.elsevier.com/retrieve/pii/S0959-4388(07)00121-3|ref=refAiran2007}} |
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*{{cite journal |author=Alilain, W. J. |title=Light-induced rescue of breathing after spinal cord injury |journal=J. Neurosci. |volume=28 |issue=46 |pages=11862–70 |date=November 2008 |pmid=19005051 |pmc=2615537 |doi=10.1523/JNEUROSCI.3378-08.2008 | |
*{{cite journal |author=Alilain, W. J. |title=Light-induced rescue of breathing after spinal cord injury |journal=J. Neurosci. |volume=28 |issue=46 |pages=11862–70 |date=November 2008 |pmid=19005051 |pmc=2615537 |doi=10.1523/JNEUROSCI.3378-08.2008 |pmid=19005051 |last2=Li |first2=X. |last3=Horn |first3=K. P. |display-authors=4 |last4=Dhingra |first4=R. |last5=Dick |first5=T. E. |last6=Herlitze |first6=S. |last7=Silver |first7=J.|ref=refAlilain2008}} |
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*{{cite journal |author=Arenkiel, B. R. |title=In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2 |journal=Neuron |volume=54 |issue=2 |pages=205–18 |date=April 2007 |pmid=17442243 |doi=10.1016/j.neuron.2007.03.005 |url=http://linkinghub.elsevier.com/retrieve/pii/S0896-6273(07)00183-3 |last2=Peca |first2=J. |last3=Davison |first3=I. G. |display-authors=4 |last4=Feliciano |first4=Catia |last5=Deisseroth |first5=Karl |last6=Augustine |first6=George J. |last7=Ehlers |first7=Michael D. |last8=Feng |first8=Guoping|ref=refArenkiel2007}} |
*{{cite journal |author=Arenkiel, B. R. |title=In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2 |journal=Neuron |volume=54 |issue=2 |pages=205–18 |date=April 2007 |pmid=17442243 |doi=10.1016/j.neuron.2007.03.005 |url=http://linkinghub.elsevier.com/retrieve/pii/S0896-6273(07)00183-3 |last2=Peca |first2=J. |last3=Davison |first3=I. G. |display-authors=4 |last4=Feliciano |first4=Catia |last5=Deisseroth |first5=Karl |last6=Augustine |first6=George J. |last7=Ehlers |first7=Michael D. |last8=Feng |first8=Guoping|ref=refArenkiel2007}} |
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*{{cite journal |author1=Atasoy, D. |author2=Aponte, Y. |author3=Su, H. H. |author4=Sternson, S. M. |title=A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping |journal=J. Neurosci. |volume=28 |issue=28 |pages=7025–30 |date=July 2008 |pmid=18614669 |pmc=2593125 |doi=10.1523/JNEUROSCI.1954-08.2008 |
*{{cite journal |author1=Atasoy, D. |author2=Aponte, Y. |author3=Su, H. H. |author4=Sternson, S. M. |title=A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping |journal=J. Neurosci. |volume=28 |issue=28 |pages=7025–30 |date=July 2008 |pmid=18614669 |pmc=2593125 |doi=10.1523/JNEUROSCI.1954-08.2008 }} |
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*{{cite journal |author1=Ayling, O. G. |author2=Harrison, T. C. |author3=Boyd, J. D. |author4=Goroshkov, A. |author5=Murphy, T. H. |title=Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice |journal=Nat. Methods |volume=6 |issue=3 |pages=219–24 |date=March 2009 |pmid=19219033 |doi=10.1038/nmeth.1303|ref=refAyling2009}} |
*{{cite journal |author1=Ayling, O. G. |author2=Harrison, T. C. |author3=Boyd, J. D. |author4=Goroshkov, A. |author5=Murphy, T. H. |title=Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice |journal=Nat. Methods |volume=6 |issue=3 |pages=219–24 |date=March 2009 |pmid=19219033 |doi=10.1038/nmeth.1303|ref=refAyling2009}} |
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*{{cite journal|last=Berndt|first=A.|author2=Yizhar, O. |author3=Gunaydin, L. A. |author4=Hegemann, P. |author5= Deisseroth, K. |title=Bi-stable neural state switches|journal=Nature Neuroscience|date=February 2009|volume=12|issue=2|pages=229–34|pmid=19079251|url=http://www.nature.com/neuro/journal/v12/n2/full/nn.2247.html|doi=10.1038/nn.2247|ref=refBerndt2009}} |
*{{cite journal|last=Berndt|first=A.|author2=Yizhar, O. |author3=Gunaydin, L. A. |author4=Hegemann, P. |author5= Deisseroth, K. |title=Bi-stable neural state switches|journal=Nature Neuroscience|date=February 2009|volume=12|issue=2|pages=229–34|pmid=19079251|url=http://www.nature.com/neuro/journal/v12/n2/full/nn.2247.html|doi=10.1038/nn.2247|ref=refBerndt2009}} |
Revision as of 04:56, 17 September 2016
Optogenetics (from Greek optikós] 'seen, visible') is a biological technique which involves the use of light to control cells in living tissue, typically neurons, that have been genetically modified to express light-sensitive ion channels. It is a neuromodulation method employed in neuroscience that uses a combination of techniques from optics and genetics to control and monitor the activities of individual neurons in living tissue—even within freely-moving animals—and to precisely measure the effects of those manipulations in real-time.[1] The key reagents used in optogenetics are light-sensitive proteins. Neuronal control is achieved using optogenetic actuators like channelrhodopsin, halorhodopsin, and archaerhodopsin, while optical recording of neuronal activities can be made with the help of optogenetic sensors for calcium (GCaMP), vesicular release (synaptopHluorin), neurotransmitter (GluSnFRs), or membrane voltage (Arclightning, ASAP1).[2] [3] Control or recording is confined to genetically defined neurons and performed in a spatiotemporally precise manner by light.
The earliest approaches for optogenetic control were developed and applied by Boris Zemelman and Gero Miesenböck,[4][5] at the Sloan-Kettering Cancer Center in New York City, and Dirk Trauner, Richard Kramer and Ehud Isacoff at the University of California, Berkeley; these methods conferred light sensitivity but were never reported to be useful by other laboratories due to the multiple components these approaches required. A distinct single-component approach involving microbial opsin genes introduced in 2005 turned out to be widely applied, as described below. Optogenetics is known for the high spatial and temporal resolution that it provides in altering the activity of specific types of neurons to control a subject's behaviour.
In 2010, optogenetics was chosen as the "Method of the Year" across all fields of science and engineering by the interdisciplinary research journal Nature Methods.[6] At the same time, optogenetics was highlighted in the article on "Breakthroughs of the Decade" in the academic research journal Science.[7] These journals also referenced recent public-access general-interest video Method of the year video and textual SciAm summaries of optogenetics.
History
The "far-fetched" possibility of using light for selectively controlling precise neural activity (action potential) patterns within subtypes of cells in the brain was articulated by Francis Crick in his Kuffler Lectures at the University of California in San Diego in 1999.[8] An early use of light to activate neurons was carried out by Richard Fork[9] who demonstrated laser activation of neurons within intact tissue, although not in a genetically-targeted manner. The earliest genetically targeted method, which used light to control genetically-sensitised neurons, was reported in January 2002 by Boris Zemelman (now at UT Austin) and Gero Miesenböck, who employed Drosophila rhodopsin photoreceptors for controlling neural activity in cultured mammalian neurons.[4] In 2003 Zemelman and Miesenböck developed a second method for light-dependent activation of neurons in which single ionotropic channels TRPV1, TRPM8 and P2X2 were gated by caged ligands in response to light.[5] Beginning in 2004, the Kramer and Isacoff groups developed organic photoswitches or "reversibly caged" compounds in collaboration with the Trauner group that could interact with genetically introduced ion channels.[10][11] However, these earlier approaches were not applied outside the original laboratories, likely because of technical challenges in delivering the multiple component parts required.
Dr. Zhuo-Hua Pan of Wayne State University, researching on restore sight to blindness, thought about using channelrhodopsin when it came out in late 2003. By February 2004, he was trying channelrhodopsin out in ganglion cells — the neurons in our eyes that connect directly to the brain — that he had cultured in a dish. They became electrically active in response to light. Over the moon with excitement, Pan applied for a grant from the National Institutes of Health. The NIH awarded him $300,000, with the comment that his research was "quite an unprecedented, highly innovative proposal, bordering on the unknown."[12]
In April 2005, Susana Lima and Miesenböck reported the first use of genetically-targeted P2X2 photostimulation to control the behaviour of an animal.[13] They showed that photostimulation of genetically circumscribed groups of neurons, such as those of the dopaminergic system, elicited characteristic behavioural changes in fruit flies. In August 2005, Karl Deisseroth's laboratory in the Bioengineering Department at Stanford including graduate students Ed Boyden and Feng Zhang (both now at MIT) published the first demonstration of a single-component optogenetic system, beginning in cultured mammalian neurons.[14][15] using channelrhodopsin, a single-component light-activated cation channel from unicellular algae, whose molecular identity and principal properties rendering it useful for optogenetic studies had been first reported in November 2003 by Georg Nagel.[16] The groups of Gottschalk and Nagel were the first to extend the usability of Channelrhodopsin-2 for controlling neuronal activity to the intact animal by showing that motor patterns in the roundworm Caenorhabditis elegans could be evoked by targeted expression and stimulation of Channelrhodopsin-2 in selected neural circuits (published in December 2005).[17] Now optogenetics has been routinely combined with brain region-and cell type-specific Cre/loxP genetic methods developed for Neuroscience by Joe Z. Tsien back in 1990s [18] to activate or inhibit specific brain regions and cell-types in vivo.[19]
The primary tools for optogenetic recordings have been genetically encoded calcium indicators (GECIs). The first GECI to be used to image activity in an animal was cameleon, designed by Atsushi Miyawaki, Roger Tsien and coworkers.[20] Cameleon was first used successfully in an animal by Rex Kerr, William Schafer and coworkers to record from neurons and muscle cells of the nematode C. elegans.[21] Cameleon was subsequently used to record neural activity in flies[22] and zebrafish.[23] In mammals, the first GECI to be used in vivo was GCaMP,[24] first developed by Nakai and coworkers.[25] GCaMP has undergone numerous improvements, and GCaMP6[26] in particular has become widely used throughout neuroscience.
In 2010 Karl Deisseroth at Stanford University was awarded the inaugural HFSP Nakasone Award "for his pioneering work on the development of optogenetic methods for studying the function of neuronal networks underlying behavior". In 2012 Gero Miesenböck was awarded the InBev-Baillet Latour International Health Prize for "pioneering optogenetic approaches to manipulate neuronal activity and to control animal behaviour." In 2013 Ernst Bamberg, Ed Boyden, Karl Deisseroth, Peter Hegemann, Gero Miesenböck and Georg Nagel were awarded The Brain Prize for "their invention and refinement of optogenetics."[27][28]
Description
Millisecond-scale temporal precision is central to optogenetics, which allows the experimenter to keep pace with fast biological information processing (for example, in probing the causal role of specific action potential patterns in defined neurons). Indeed, to probe the neural code, optogenetics by definition must operate on the millisecond timescale to allow addition or deletion of precise activity patterns within specific cells in the brains of intact animals, including mammals (see Figure 1). By comparison, the temporal precision of traditional genetic manipulations (employed to probe the causal role of specific genes within cells, via "loss-of-function" or "gain of function" changes in these genes) is rather slow, from hours or days to months. It is important to also have fast readouts in optogenetics that can keep pace with the optical control. This can be done with electrical recordings ("optrodes") or with reporter proteins that are biosensors, where scientists have fused fluorescent proteins to detector proteins. An example of this is voltage-sensitive fluorescent protein (VSFP2).[32]
The hallmark of optogenetics therefore is introduction of fast light-activated channels and enzymes that allow temporally precise manipulation of electrical and biochemical events while maintaining cell-type resolution through the use of specific targeting mechanisms. Among the microbial opsins which can be used to investigate the function of neural systems are the channelrhodopsins (ChR2, ChR1, VChR1, and SFOs) to excite neurons. For silencing, halorhodopsin (NpHR),[33] enhanced halorhodopsins (eNpHR2.0 and eNpHR3.0),[34] archaerhodopsin (Arch), Leptosphaeria maculans fungal opsins (Mac), and enhanced bacteriorhodopsin (eBR) have been employed to inhibit neurons (see Figure 2), including in freely-moving mammals.[35]
Moreover, optogenetic control of well-defined biochemical events within behaving mammals is now also possible. Building on prior work fusing vertebrate opsins to specific G-protein coupled receptors [36] a family of chimeric single-component optogenetic tools was created that allowed researchers to manipulate within behaving mammals the concentration of defined intracellular messengers such as cAMP and IP3 in targeted cells [37] Other biochemical approaches to optogenetics (crucially, with tools that displayed low activity in the dark) followed soon thereafter, when optical control over small GTPases and adenylyl cyclases was achieved in cultured cells using novel strategies from several different laboratories.[38][39][40][41][42] This emerging repertoire of optogenetic probes now allows cell-type-specific and temporally precise control of multiple axes of cellular function within intact animals.[43]
Optogenetics also necessarily includes 1) the development of genetic targeting strategies such as cell-specific promoters or other customized conditionally-active viruses, to deliver the light-sensitive probes to specific populations of neurons in the brain of living animals (e.g. worms, fruit flies, mice, rats, and monkeys), and 2) hardware (e.g. integrated fiberoptic and solid-state light sources) to allow specific cell types, even deep within the brain, to be controlled in freely behaving animals. Most commonly, the latter is now achieved using the fiberoptic-coupled diode technology introduced in 2007,[44][45][46] though to avoid use of implanted electrodes, researchers have engineered ways to inscribe a "window" made of zirconia that has been modified to be transparent and implanted in mice skulls, to allow optical waves to penetrate more deeply to stimulate or inhibit individual neurons.[47]
To stimulate superficial brain areas such as the cerebral cortex, optical fibers or LEDs can be directly mounted to the skull of the animal. More deeply implanted optical fibers have been used to deliver light to deeper brain areas. Complementary to fiber-tethered approaches, completely wireless techniques have been developed utilizing wirelessly delivered power to headborne LEDs for unhindered study of complex behaviors in freely behaving vertebrates.[48] In invertebrates such as worms and fruit flies some amount of retinal isomerase all-trans-retinal (ATR) is supplemented with food. A key advantage of microbial opsins as noted above is that they are fully functional without the addition of exogenous co-factors in vertebrates.
The field of optogenetics has furthered the fundamental scientific understanding of how specific cell types contribute to the function of biological tissues such as neural circuits in vivo (see references from the scientific literature below). Moreover, on the clinical side, optogenetics-driven research has led to insights into Parkinson's disease[49][50] and other neurological and psychiatric disorders. Indeed, optogenetics papers in 2009 have also provided insight into neural codes relevant to autism, Schizophrenia, drug abuse, anxiety, and depression.[35][51][52][53]
It has been pointed out that beyond its scientific impact, optogenetics also represents an important case study in the value of both ecological conservation (as many of the key tools of optogenetics arise from microbial organisms occupying specialized environmental niches), and in the importance of pure basic science (as these opsins were studied over decades for their own sake by biophysicists and microbiologists, without involving consideration of their potential value in delivering insights into neuroscience and neuropsychiatric disease).
Applications
Optogenetic activation and/or silencing has been used at least in the following regions:
Amygdala
Optogenetic approaches have been used to map neural circuits in the amygdala that contribute to fear conditioning.[54][55][56][57]
Olfactory Bulb
Optogenetic activation of olfactory sensory neurons was critical for demonstrating timing in odor processing [58] and for mechanism of neuromodulatory mediated olfactory guided behaviors (e.g. aggression, mating) [59]
Nucleus accumbens
Optogenetics, freely moving mammalian behavior, in vivo electrophysiology, and slice physiology have been integrated to probe the cholinergic interneurons of the nucleus accumbens by direct excitation or inhibition. Despite representing less than 1% of the total population of accumbal neurons, these cholinergic cells are able to control the activity of the dopaminergic terminals that innervate medium spiny neurons (MSNs) in the nucleus accumbens.[60] These accumbal MSNs are known to be involved in the neural pathway through which cocaine exerts its effects, because decreasing cocaine-induced changes in the activity of these neurons has been shown to inhibit cocaine conditioning. The few cholinergic neurons present in the nucleus accumbens may prove viable targets for pharmacotherapy in the treatment of cocaine dependence[35]
Prefrontal cortex
In vivo and in vitro recordings (by the Cooper laboratory) of individual CAMKII AAV-ChR2 expressing pyramidal neurons within the prefrontal cortex demonstrated high fidelity action potential output with short pulses of blue light at 20 Hz (Figure 1).[29] The same group recorded complete green light-induced silencing of spontaneous activity in the same prefrontal cortical neuronal population expressing an AAV-NpHR vector (Figure 2).[29]
Atrial fibrillation
Optogenetics on atrial cardiomyocytes was used as atrial fibrillation to end spiral wave arrhythmias with light.[61] This method is still in the development stage.
Spiral ganglion
Optogenetic stimulation of spiral ganglion in deaf mice restored auditory activity.[62]
Brainstem
Optogenetic stimulation of a modified red-light excitable channelrhodopsin (ReaChR) expressed in the facial motor nucleus enabled minimally invasive activation of motoneurons effective in driving whisker movements in mice.[63]
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Additional reading
This 'further reading' section may need cleanup. (August 2014) |
- Airan, R. D.; Hu, E. S.; Vijaykumar, R.; Roy, M.; Meltzer, L. A.; Deisseroth, K. (October 2007). "Integration of light-controlled neuronal firing and fast circuit imaging". Current Opinion in Neurobiology. 17 (5): 587–92. doi:10.1016/j.conb.2007.11.003. PMID 18093822.
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- Ayling, O. G.; Harrison, T. C.; Boyd, J. D.; Goroshkov, A.; Murphy, T. H. (March 2009). "Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice". Nat. Methods. 6 (3): 219–24. doi:10.1038/nmeth.1303. PMID 19219033.
- Berndt, A.; Yizhar, O.; Gunaydin, L. A.; Hegemann, P.; Deisseroth, K. (February 2009). "Bi-stable neural state switches". Nature Neuroscience. 12 (2): 229–34. doi:10.1038/nn.2247. PMID 19079251.
- Bi, A.; Cui, J.; Ma, Y. P.; Olshevskaya, Elena; et al. (April 2006). "Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration". Neuron. 50 (1): 23–33. doi:10.1016/j.neuron.2006.02.026. PMC 1459045. PMID 16600853.
- Busskamp, V. (2010-07-23). "Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa". Science. 329 (5990): 413–7. Bibcode:2010Sci...329..413B. doi:10.1126/science.1190897. PMID 20576849.
{{cite journal}}
: Unknown parameter|coauthors=
ignored (|author=
suggested) (help) - Cardin, J. A.; Carlén, M.; Meletis, K.; Knoblich, U.; Zhang, F.; Deisseroth, K.; Tsai, L. H.; Moore, C. I. (2010). "Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2". Nature protocols. 5 (2): 247–54. doi:10.1038/nprot.2009.228. PMID 20134425.
- Carter, M. E.; Adamantidis, A.; Ohtsu, H.; Deisseroth, K.; de Lecea, L. (2009-09-02). "Sleep homeostasis modulates hypocretin-mediated sleep-to-wake transitions". Journal of Neuroscience. 29 (35): 10939–49. doi:10.1523/JNEUROSCI.1205-09.2009. PMID 19726652.
- Carter, M. E.; Yizhar, O.; Chikahisa, S.; Nguyen, H.; Adamantidis, A.; Nishino, S.; Deisseroth, K.; de Lecea, L. (December 2010). "Tuning arousal with optogenetic modulation of locus coeruleus neurons". Nature Neuroscience. 13 (12): 1526–33. doi:10.1038/nn.2682. PMC 3174240. PMID 21037585.
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- Deisseroth, Karl. "Optogenetics: Controlling the Brain with Light".
- Diester, I.; Kaufman, M. T.; Mogri, M.; Pashaie, R.; Goo, W.; Yizhar, O.; Ramakrishnan, C.; Deisseroth, K.; Shenoy, K. V. (March 2011). "An optogenetic toolbox designed for primates". Nature Neuroscience. 14 (3): 387–97. doi:10.1038/nn.2749. PMC 3150193. PMID 21278729.
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: CS1 maint: multiple names: authors list (link) CS1 maint: unflagged free DOI (link) - Han, X.; Qian, X.; Bernstein, J. G.; Zhou, Hui-hui; et al. (April 2009). "Millisecond-timescale optical control of neural dynamics in the nonhuman primate brain". Neuron. 62 (2): 191–8. doi:10.1016/j.neuron.2009.03.011. PMC 2830644. PMID 19409264.
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- Lee, J. H.; Durand, R.; Gradinaru, V.; Zhang, F.; Goshen, I.; Kim, D. S.; Fenno, L. E.; Ramakrishnan, C.; Deisseroth, K. (2010-06-10). "Global and local fMRI signals driven by neurons defined optogenetically by type and wiring". Nature. 465 (7299): 788–92. Bibcode:2010Natur.465..788L. doi:10.1038/nature09108. PMC 3177305. PMID 20473285.
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: CS1 maint: multiple names: authors list (link) - Llewellyn, M. E.; Thompson, K. R.; Deisseroth, K.; Delp, S. L. (October 2010). "Orderly recruitment of motor units under optical control in vivo". Nature Medicine. 16 (10): 1161–5. doi:10.1038/nm.2228. PMID 20871612.
- Lobo, M. K. (2010-10-15). "Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward". Science. 330 (6002): 385–90. Bibcode:2010Sci...330..385L. doi:10.1126/science.1188472. PMC 3011229. PMID 20947769.
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ignored (|author=
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: Unknown parameter|coauthors=
ignored (|author=
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: CS1 maint: unflagged free DOI (link)
External links
This article's use of external links may not follow Wikipedia's policies or guidelines. (October 2013) |
- Optogenetics Resource Center, maintained by the Deisseroth lab.
- Synthetic Neurobiology Group, MIT, the portal of the Boyden lab.
- OpenOptogenetics.org, an optogenetics wiki, and its companion blog.
- Molecular Neurogenetics and Optophysiology Laboratory,"Optogenetic activation and silencing recordings of individual prefrontal cortical neurons in vivo and in vitro.
- Sohal lab portal
- Nurmikko lab portal
- Lab of Dr. Zhuo-Hua Pan
- Optophysiology at the Tyler lab
- Video: Ed Boyden on Optogenetics -- selective brain stimulation with light (SPIE Newsroom, April 2011)