1932

Abstract

Genetically encoded tools for visualizing and manipulating neurons in vivo have led to significant advances in neuroscience, in large part because of the ability to target expression to specific cell populations of interest. Current methods enable targeting based on marker gene expression, development, anatomical projection pattern, synaptic connectivity, and recent activity as well as combinations of these factors. Here, we review these methods, focusing on issues of practical implementation as well as areas for future improvement.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-120215-035011
2016-11-23
2024-06-13
Loading full text...

Full text loading...

/deliver/fulltext/genet/50/1/annurev-genet-120215-035011.html?itemId=/content/journals/10.1146/annurev-genet-120215-035011&mimeType=html&fmt=ahah

Literature Cited

  1. Adamantidis AR, Tsai H-C, Boutrel B, Zhang F, Stuber GD. 1.  et al. 2011. Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J. Neurosci. 31:3010829–35 [Google Scholar]
  2. Armbruster BN, Li X, Pausch MH, Herlitze S, Roth BL. 2.  2007. Evolving the lock to fit the key to create a family of G protein–coupled receptors potently activated by an inert ligand. PNAS 104:125163–68 [Google Scholar]
  3. Aso Y, Hattori D, Yu Y, Johnston RM, Iyer NA. 3.  et al. 2014. The neuronal architecture of the mushroom body provides a logic for associative learning. eLife 3:e04577 [Google Scholar]
  4. Atasoy D, Aponte Y, Su HH, Sternson SM. 4.  2008. A FLEX switch targets channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J. Neurosci. 28:287025–30 [Google Scholar]
  5. Awatramani R, Soriano P, Rodriguez C, Mai JJ, Dymecki SM. 5.  2003. Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nat. Genet. 35:170–75 [Google Scholar]
  6. Ayre BG, Köhler U, Goodman HM, Haseloff J. 6.  1999. Design of highly specific cytotoxins by using trans-splicing ribozymes. PNAS 96:73507–12 [Google Scholar]
  7. Bäckman CM, Malik N, Zhang Y, Shan L, Grinberg A. 7.  et al. 2006. Characterization of a mouse strain expressing Cre recombinase from the 3′ untranslated region of the dopamine transporter locus. Genesis 44:8383–90 [Google Scholar]
  8. Banghart M, Borges K, Isacoff E, Trauner D, Kramer RH. 8.  2004. Light-activated ion channels for remote control of neuronal firing. Nat. Neurosci. 7:121381–86 [Google Scholar]
  9. Beier KT, Saunders A, Oldenburg IA, Miyamichi K, Akhtar N. 9.  et al. 2011. Anterograde or retrograde transsynaptic labeling of CNS neurons with vesicular stomatitis virus vectors. PNAS 108:3715414–19 [Google Scholar]
  10. Beier KT, Saunders AB, Oldenburg IA, Sabatini BL, Cepko CL. 10.  2013. Vesicular stomatitis virus with the rabies virus glycoprotein directs retrograde transsynaptic transport among neurons in vivo. Front. Neural Circuits 7:11 [Google Scholar]
  11. Bellen HJ. 11.  1999. Ten years of enhancer detection: lessons from the fly. Plant Cell 11:122271–81 [Google Scholar]
  12. Bellen HJ, O'Kane CJ, Wilson C, Grossniklaus U, Pearson RK, Gehring WJ. 12.  1989. P-element–mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev. 3:91288–300 [Google Scholar]
  13. Bidaye SS, Machacek C, Wu Y, Dickson BJ. 13.  2014. Neuronal control of Drosophila walking direction. Science 344:617997–101 [Google Scholar]
  14. Bier E, Vaessin H, Shepherd S, Lee K, McCall K. 14.  et al. 1989. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 3:91273–87 [Google Scholar]
  15. Bischof J, Maeda RK, Hediger M, Karch F, Basler K. 15.  2007. An optimized transgenesis system for Drosophila using germ-line–specific phiC31 integrases. PNAS 104:93312–17 [Google Scholar]
  16. Blackwood EM, Kadonaga JT. 16.  1998. Going the distance: a current view of enhancer action. Science 281:537360–63 [Google Scholar]
  17. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 17.  2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8:91263–68 [Google Scholar]
  18. Brand AH, Perrimon N. 18.  1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:2401–15 [Google Scholar]
  19. Brown BD, Venneri MA, Zingale A, Sergi Sergi L, Naldini L. 19.  2006. Endogenous microRNA regulation suppresses transgene expression in hematopoietic lineages and enables stable gene transfer. Nat. Med. 12:5585–91 [Google Scholar]
  20. Capecchi MR. 20.  1989. Altering the genome by homologous recombination. Science 244:49101288–92 [Google Scholar]
  21. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. 21.  1994. Green fluorescent protein as a marker for gene expression. Science 263:5148802–5 [Google Scholar]
  22. Chappell SA, Edelman GM, Mauro VP. 22.  2000. A 9-nt segment of a cellular mRNA can function as an internal ribosome entry site (IRES) and when present in linked multiple copies greatly enhances IRES activity. PNAS 97:41536–41 [Google Scholar]
  23. Chen R, Romero G, Christiansen MG, Mohr A, Anikeeva P. 23.  2015. Wireless magnetothermal deep brain stimulation. Science 347:62291477–80 [Google Scholar]
  24. Chow BY, Han X, Dobry AS, Qian X, Chuong AS. 24.  et al. 2010. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463:727798–102 [Google Scholar]
  25. Ciesielska A, Hadaczek P, Mittermeyer G, Zhou S, Wright JF. 25.  et al. 2013. Cerebral infusion of AAV9 vector-encoding non-self proteins can elicit cell-mediated immune responses. Mol. Ther. 21:1158–66 [Google Scholar]
  26. Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H. 26.  et al. 2009. Writing memories with light-addressable reinforcement circuitry. Cell 139:2405–15 [Google Scholar]
  27. Cong L, Ran FA, Cox D, Lin S, Barretto R. 27.  et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:6121819–23 [Google Scholar]
  28. Cooley L, Kelley R, Spradling A. 28.  1988. Insertional mutagenesis of the Drosophila genome with single P elements. Science 239:48441121–28 [Google Scholar]
  29. Cowansage KK, Shuman T, Dillingham BC, Chang A, Golshani P, Mayford M. 29.  2014. Direct reactivation of a coherent neocortical memory of context. Neuron 84:2432–41 [Google Scholar]
  30. Crittenden JR, Lacey CJ, Lee T, Bowden HA, Graybiel AM. 30.  2014. Severe drug-induced repetitive behaviors and striatal overexpression of VAChT in ChAT-ChR2-EYFP BAC transgenic mice. Front. Neural Circuits 8:57 [Google Scholar]
  31. Crocker A, Shahidullah M, Levitan IB, Sehgal A. 31.  2010. Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron 65:5670–81 [Google Scholar]
  32. Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP. 32.  1998. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 8:241323–26 [Google Scholar]
  33. DasGupta S, Ferreira CH, Miesenböck G. 33.  2014. FoxP influences the speed and accuracy of a perceptual decision in Drosophila. Science 344:6186901–4 [Google Scholar]
  34. Defelipe J, López-Cruz PL, Benavides-Piccione R, Bielza C, Larrañaga P. 34.  et al. 2013. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 14:3202–16 [Google Scholar]
  35. Deverman BE, Pravdo PL, Simpson BP, Kumar SR, Chan KY. 35.  et al. 2016. Cre-dependent selection yields AAV variants for widespread gene transfer to the adult brain. Nat. Biotechnol. 34:2204–9 [Google Scholar]
  36. Dittgen T, Nimmerjahn A, Komai S, Licznerski P, Waters J. 36.  et al. 2004. Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo. PNAS 101:5218206–11 [Google Scholar]
  37. Dix RD, McKendall RR, Baringer JR. 37.  1983. Comparative neurovirulence of herpes simplex virus type 1 strains after peripheral or intracerebral inoculation of BALB/c mice. Infect. Immun. 40:1103–12 [Google Scholar]
  38. Dong JY, Fan PD, Frizzell RA. 38.  1996. Quantitative analysis of the packaging capacity of recombinant adeno-associated virus. Hum. Gene Ther. 7:172101–12 [Google Scholar]
  39. Federspiel MJ, Bates P, Young JA, Varmus HE, Hughes SH. 39.  1994. A system for tissue-specific gene targeting: transgenic mice susceptible to subgroup A avian leukosis virus-based retroviral vectors. PNAS 91:2311241–45 [Google Scholar]
  40. Feil R, Wagner J, Metzger D, Chambon P. 40.  1997. Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem. Biophys. Res. Comm. 237:3752–57 [Google Scholar]
  41. Feldbauer K, Zimmermann D, Pintschovius V, Spitz J, Bamann C, Bamberg E. 41.  2009. Channelrhodopsin-2 is a leaky proton pump. PNAS 106:3012317–22 [Google Scholar]
  42. Fenno L, Yizhar O, Deisseroth K. 42.  2011. The development and application of optogenetics. Annu. Rev. Neurosci. 34:389–412 [Google Scholar]
  43. Fenno LE, Mattis J, Ramakrishnan C, Hyun M, Lee SY. 43.  et al. 2014. Targeting cells with single vectors using multiple-feature Boolean logic. Nat. Methods 11:7763–72 [Google Scholar]
  44. Fishell G, Rudy B. 44.  2011. Mechanisms of inhibition within the telencephalon: “where the wild things are.”. Annu. Rev. Neurosci. 34:535–67 [Google Scholar]
  45. Fosque BF, Sun Y, Dana H, Yang C-T, Ohyama T. 45.  et al. 2015. Labeling of active neural circuits in vivo with designed calcium integrators. Science 347:6223755–60 [Google Scholar]
  46. Friggi-Grelin F, Coulom H, Meller M, Gomez D, Hirsh J, Birman S. 46.  2003. Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J. Neurobiol. 54:4618–27 [Google Scholar]
  47. Furth PA, St. Onge L, Böger H, Gruss P, Gossen M. 47.  et al. 1994. Temporal control of gene expression in transgenic mice by a tetracycline-responsive promoter. PNAS 91:209302–6 [Google Scholar]
  48. Garner AR, Rowland DC, Hwang SY, Baumgaertel K, Roth BL. 48.  et al. 2012. Generation of a synthetic memory trace. Science 335:60751513–16 [Google Scholar]
  49. Gohl DM, Silies MA, Gao XJ, Bhalerao S, Luongo FJ. 49.  et al. 2011. A versatile in vivo system for directed dissection of gene expression patterns. Nat. Methods 8:3231–37 [Google Scholar]
  50. Gossen M, Bujard H. 50.  1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. PNAS 89:125547–51 [Google Scholar]
  51. Gradinaru V, Zhang F, Ramakrishnan C, Mattis J, Prakash R. 51.  et al. 2010. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141:1154–65 [Google Scholar]
  52. Greenberg ME, Ziff EB, Greene LA. 52.  1986. Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science 234:477280–83 [Google Scholar]
  53. Gu H, Marth JD, Orban PC, Mossmann H, Rajewsky K. 53.  1994. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science 265:5168103–6 [Google Scholar]
  54. Guenthner CJ, Miyamichi K, Yang HH, Heller HC, Luo L. 54.  2013. Permanent genetic access to transiently active neurons via TRAP: targeted recombination in active populations. Neuron 78:5773–84 [Google Scholar]
  55. Guggenhuber S, Monory K, Lutz B, Klugmann M. 55.  2010. AAV vector-mediated overexpression of CB1 cannabinoid receptor in pyramidal neurons of the hippocampus protects against seizure-induced excitoxicity. PLOS ONE 5:12e15707 [Google Scholar]
  56. Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A. 56.  et al. 2008. An internal thermal sensor controlling temperature preference in Drosophila. Nature 454:7201217–20 [Google Scholar]
  57. Harper SM, Neil LC, Gardner KH. 57.  2003. Structural basis of a phototropin light switch. Science 301:56391541–44 [Google Scholar]
  58. Hayashi I, Mizuno H, Tong KI, Furuta T, Tanaka F. 58.  et al. 2007. Crystallographic evidence for water-assisted photo-induced peptide cleavage in the stony coral fluorescent protein Kaede. J. Mol. Biol. 372:4918–26 [Google Scholar]
  59. Hayashi S, Ito K, Sado Y, Taniguchi M, Akimoto A. 59.  et al. 2002. GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 34:1–258–61 [Google Scholar]
  60. Hayashi-Takagi A, Yagishita S, Nakamura M, Shirai F, Wu YI. 60.  et al. 2015. Labelling and optical erasure of synaptic memory traces in the motor cortex. Nature 525:7569333–38 [Google Scholar]
  61. Heim R, Tsien RY. 61.  1996. Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr. Biol. 6:2178–82 [Google Scholar]
  62. Heintz N. 62.  2001. BAC to the future: the use of BAC transgenic mice for neuroscience research. Nat. Rev. Neurosci. 2:12861–70 [Google Scholar]
  63. Hikida T, Kimura K, Wada N, Funabiki K, Nakanishi S. 63.  2010. Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior. Neuron 66:6896–907 [Google Scholar]
  64. Hutson TH, Kathe C, Moon LDF. 64.  2016. Trans-neuronal transduction of spinal neurons following cortical injection and anterograde axonal transport of a bicistronic AAV1 vector. Gene Ther 23:2231–36 [Google Scholar]
  65. Jenett A, Rubin GM, Ngo TT, Shepherd D, Murphy C. 65.  et al. 2012. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep 2:4991–1001 [Google Scholar]
  66. Jennings JH, Sparta DR, Stamatakis AM, Ung RL, Pleil KE. 66.  et al. 2013. Distinct extended amygdala circuits for divergent motivational states. Nature 496:7444224–28 [Google Scholar]
  67. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 67.  2012. A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science 337:6096816–21 [Google Scholar]
  68. Jung MW, McNaughton BL. 68.  1993. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3:2165–82 [Google Scholar]
  69. Kätzel D, Zemelman BV, Buetfering C, Wölfel M, Miesenböck G. 69.  2011. The columnar and laminar organization of inhibitory connections to neocortical excitatory cells. Nat. Neurosci. 14:1100–7 [Google Scholar]
  70. Kawashima T, Kitamura K, Suzuki K, Nonaka M, Kamijo S. 70.  et al. 2013. Functional labeling of neurons and their projections using the synthetic activity-dependent promoter E-SARE. Nat. Methods 10:9889–95 [Google Scholar]
  71. Kennedy MJ, Hughes RM, Peteya LA, Schwartz JW, Ehlers MD, Tucker CL. 71.  2010. Rapid blue-light–mediated induction of protein interactions in living cells. Nat. Methods 7:12973–75 [Google Scholar]
  72. Kim CH, Oh Y, Lee TH. 72.  1997. Codon optimization for high-level expression of human erythropoietin (EPO) in mammalian cells. Gene 199:1–2293–301 [Google Scholar]
  73. Kim JH, Lee S-R, Li L-H, Park H-J, Park J-H. 73.  et al. 2011. High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLOS ONE 6:4e18556 [Google Scholar]
  74. Kitamoto T. 74.  2001. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47:281–92 [Google Scholar]
  75. Kohatsu S, Koganezawa M, Yamamoto D. 75.  2011. Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69:3498–508 [Google Scholar]
  76. Kolisnyk B, Guzman MS, Raulic S, Fan J, Magalhães AC. 76.  et al. 2013. ChAT-ChR2-EYFP mice have enhanced motor endurance but show deficits in attention and several additional cognitive domains. J. Neurosci. 33:2510427–38 [Google Scholar]
  77. Kramer PF, Christensen CH, Hazelwood LA, Dobi A, Bock R. 77.  et al. 2011. Dopamine D2 receptor overexpression alters behavior and physiology in Drd2-EGFP mice. J. Neurosci. 31:1126–32 [Google Scholar]
  78. Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, Waddell S. 78.  2009. A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139:2416–27 [Google Scholar]
  79. Kremer EJ, Boutin S, Chillon M, Danos O. 79.  2000. Canine adenovirus vectors: an alternative for adenovirus-mediated gene transfer. J. Virol. 74:1505–12 [Google Scholar]
  80. Kuhlman SJ, Huang ZJ. 80.  2008. High-resolution labeling and functional manipulation of specific neuron types in mouse brain by Cre-activated viral gene expression. PLOS ONE 3:4e2005 [Google Scholar]
  81. Kumar M, Keller B, Makalou N, Sutton RE. 81.  2001. Systematic determination of the packaging limit of lentiviral vectors. Hum. Gene Ther. 12:151893–905 [Google Scholar]
  82. Lai SL, Lee T. 82.  2006. Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9:5703–9 [Google Scholar]
  83. Lakso M, Sauer B, Mosinger B, Lee EJ, Manning RW. 83.  et al. 1992. Targeted oncogene activation by site-specific recombination in transgenic mice. PNAS 89:146232–36 [Google Scholar]
  84. Lammel S, Steinberg EE, Földy C, Wall NR, Beier K. 84.  et al. 2015. Diversity of transgenic mouse models for selective targeting of midbrain dopamine neurons. Neuron 85:2429–38 [Google Scholar]
  85. Langevin LM, Mattar P, Scardigli R, Roussigné M, Logan C. 85.  et al. 2007. Validating in utero electroporation for the rapid analysis of gene regulatory elements in the murine telencephalon. Dev. Dyn. 236:51273–86 [Google Scholar]
  86. Lechner HA, Lein ES, Callaway EM. 86.  2002. A genetic method for selective and quickly reversible silencing of mammalian neurons. J. Neurosci. 22:135287–90 [Google Scholar]
  87. Lee AT, Gee SM, Vogt D, Patel T, Rubenstein JL, Sohal VS. 87.  2014. Pyramidal neurons in prefrontal cortex receive subtype-specific forms of excitation and inhibition. Neuron 81:161–68 [Google Scholar]
  88. Lee T, Luo L. 88.  1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:3451–61 [Google Scholar]
  89. Li X, Gutierrez DV, Hanson MG, Han J, Mark MD. 89.  et al. 2005. Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. PNAS 102:4917816–21 [Google Scholar]
  90. Lima SQ, Miesenböck G. 90.  2005. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121:1141–52 [Google Scholar]
  91. Lin AC, Bygrave AM, de Calignon A, Lee T, Miesenböck G. 91.  2014. Sparse, decorrelated odor coding in the mushroom body enhances learned odor discrimination. Nat. Neurosci. 17:4559–68 [Google Scholar]
  92. Lin JY, Sann SB, Zhou K, Nabavi S, Proulx CD. 92.  et al. 2013. Optogenetic inhibition of synaptic release with chromophore-assisted light inactivation (CALI). Neuron 79:2241–53 [Google Scholar]
  93. Liu X, Ramirez S, Pang PT, Puryear CB, Govindarajan A. 93.  et al. 2012. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484:7394381–85 [Google Scholar]
  94. Lo L, Anderson DJ. 94.  2011. A Cre-dependent, anterograde transsynaptic viral tracer for mapping output pathways of genetically marked neurons. Neuron 72:6938–50 [Google Scholar]
  95. Luan H, Peabody NC, Vinson CR, White BH. 95.  2006. Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 52:3425–36 [Google Scholar]
  96. Luo L, Callaway EM, Svoboda K. 96.  2008. Genetic dissection of neural circuits. Neuron 57:5634–60 [Google Scholar]
  97. Ma J, Ptashne M. 97.  1987. The carboxy-terminal 30 amino acids of GAL4 are recognized by GAL80. Cell 50:1137–42 [Google Scholar]
  98. Machold R, Fishell G. 98.  2005. Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48:117–24 [Google Scholar]
  99. Madisen L, Garner AR, Shimaoka D, Chuong AS, Klapoetke NC. 99.  et al. 2015. Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance. Neuron 85:5942–58 [Google Scholar]
  100. Madisen L, Mao T, Koch H, Zhuo JM, Berenyi A. 100.  et al. 2012. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 15:5793–802 [Google Scholar]
  101. Magnus CJ, Lee PH, Atasoy D, Su HH, Looger LL, Sternson SM. 101.  2011. Chemical and genetic engineering of selective ion channel–ligand interactions. Science 333:60471292–96 [Google Scholar]
  102. Manseau L, Baradaran A, Brower D, Budhu A, Elefant F. 102.  et al. 1997. GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev. Dyn. 209:3310–22 [Google Scholar]
  103. Marshel JH, Mori T, Nielsen KJ, Callaway EM. 103.  2010. Targeting single neuronal networks for gene expression and cell labeling in vivo. Neuron 67:4562–74 [Google Scholar]
  104. Maston GA, Evans SK, Green MR. 104.  2006. Transcriptional regulatory elements in the human genome. Annu. Rev. Genom. Hum. Genet. 7:129–59 [Google Scholar]
  105. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. 105.  2003. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302:56511765–68 [Google Scholar]
  106. Metzger D, Clifford J, Chiba H, Chambon P. 106.  1995. Conditional site-specific recombination in mammalian cells using a ligand-dependent chimeric Cre recombinase. PNAS 92:156991–95 [Google Scholar]
  107. Miesenböck G. 107.  2011. Optogenetic control of cells and circuits. Annu. Rev. Cell Dev. Biol. 27:731–58 [Google Scholar]
  108. Miesenböck G. 108.  2009. The optogenetic catechism. Science 326:5951395–99 [Google Scholar]
  109. Miesenböck G, De Angelis DA, Rothman JE. 109.  1998. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:6689192–95 [Google Scholar]
  110. Miesenböck G, Kevrekidis IG. 110.  2005. Optical imaging and control of genetically designated neurons in functioning circuits. Annu. Rev. Neurosci. 28:533–63 [Google Scholar]
  111. Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA. 111.  et al. 1997. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388:6645882–87 [Google Scholar]
  112. Morgan JI, Curran T. 112.  1986. Role of ion flux in the control of c-fos expression. Nature 322:6079552–55 [Google Scholar]
  113. Müller OJ, Kaul F, Weitzman MD, Pasqualini R, Arap W. 113.  et al. 2003. Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors. Nat. Biotechnol. 21:91040–46 [Google Scholar]
  114. Nakai J, Ohkura M, Imoto K. 114.  2001. A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nat. Biotechnol. 19:2137–41 [Google Scholar]
  115. Naldini L, Blomer U, Gage FH, Trono D, Verma IM. 115.  1996. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. PNAS 93:2111382–88 [Google Scholar]
  116. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R. 116.  et al. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:5259263–67 [Google Scholar]
  117. Nathanson JL, Jappelli R, Scheeff ED, Manning G, Obata K. 117.  et al. 2009. Short promoters in viral vectors drive selective expression in mammalian inhibitory neurons, but do not restrict activity to specific inhibitory cell-types. Front. Neural Circuits 3:19 [Google Scholar]
  118. Ochman H, Gerber AS, Hartl DL. 118.  1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120:3621–23 [Google Scholar]
  119. Oh MS, Hong SJ, Huh Y, Kim K-S. 119.  2009. Expression of transgenes in midbrain dopamine neurons using the tyrosine hydroxylase promoter. Gene Ther 16:3437–40 [Google Scholar]
  120. O'Keefe J, Dostrovsky J. 120.  1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:1171–75 [Google Scholar]
  121. Oyibo HK, Znamenskiy P, Oviedo HV, Enquist LW, Zador AM. 121.  2014. Long-term Cre-mediated retrograde tagging of neurons using a novel recombinant pseudorabies virus. Front. Neuroanat. 8:86 [Google Scholar]
  122. Pelletier J, Sonenberg N. 122.  1988. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334:6180320–25 [Google Scholar]
  123. 123. Petilla Interneuron Nomenclat. Group Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G et al. 2008. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9:7557–68 [Google Scholar]
  124. Petitclerc D, Attal J, Théron MC, Bearzotti M, Bolifraud P. 124.  et al. 1995. The effect of various introns and transcription terminators on the efficiency of expression vectors in various cultured cell lines and in the mammary gland of transgenic mice. J. Biotechnol. 40:3169–78 [Google Scholar]
  125. Petreanu L, Huber D, Sobczyk A, Svoboda K. 125.  2007. Channelrhodopsin-2–assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 10:5663–68 [Google Scholar]
  126. Pfeiffer BD, Jenett A, Hammonds AS, Ngo T-TB, Misra S. 126.  et al. 2008. Tools for neuroanatomy and neurogenetics in Drosophila. PNAS 105:289715–20 [Google Scholar]
  127. Pfeiffer BD, Ngo T-TB, Hibbard KL, Murphy C, Jenett A. 127.  et al. 2010. Refinement of tools for targeted gene expression in Drosophila. Genetics 186:2735–55 [Google Scholar]
  128. Potter CJ, Tasic B, Russler EV, Liang L, Luo L. 128.  2010. The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell 141:3536–48 [Google Scholar]
  129. Ramirez S, Liu X, Lin P-A, Suh J, Pignatelli M. 129.  et al. 2013. Creating a false memory in the hippocampus. Science 341:6144387–91 [Google Scholar]
  130. Rancz EA, Franks KM, Schwarz MK, Pichler B, Schaefer AT, Margrie TW. 130.  2011. Transfection via whole-cell recording in vivo: bridging single-cell physiology, genetics and connectomics. Nat. Neurosci. 14:4527–32 [Google Scholar]
  131. Reardon TR, Murray AJ, Turi GF, Wirblich C, Croce KR. 131.  et al. 2016. Rabies virus CVS-N2c(ΔG) strain enhances retrograde synaptic transfer and neuronal viability. Neuron 89:4711–24 [Google Scholar]
  132. Reijmers LG, Perkins BL, Matsuo N, Mayford M. 132.  2007. Localization of a stable neural correlate of associative memory. Science 317:58421230–33 [Google Scholar]
  133. Rodan AR, Kiger JA, Heberlein U. 133.  2002. Functional dissection of neuroanatomical loci regulating ethanol sensitivity in Drosophila. J. Neurosci. 22:219490–501 [Google Scholar]
  134. Rogan SC, Roth BL. 134.  2011. Remote control of neuronal signaling. Pharmacol. Rev. 63:2291–315 [Google Scholar]
  135. Rogers SW, Tvrdik P, Capecchi MR, Gahring LC. 135.  2012. Prenatal ablation of nicotinic receptor α7 cell lineages produces lumbosacral spina bifida the severity of which is modified by choline and nicotine exposure. Am. J. Med. Genet. 158A:51135–44 [Google Scholar]
  136. Rong YS, Golic KG. 136.  2000. Gene targeting by homologous recombination in Drosophila. Science 288:54732013–18 [Google Scholar]
  137. Rose MF, Ahmad KA, Thaller C, Zoghbi HY. 137.  2009. Excitatory neurons of the proprioceptive, interoceptive, and arousal hindbrain networks share a developmental requirement for Math1. PNAS 106:5222462–67 [Google Scholar]
  138. Rudy B, Fishell G, Lee S, Hjerling-Leffler J. 138.  2011. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71:145–61 [Google Scholar]
  139. Ryan MD, King AM, Thomas GP. 139.  1991. Cleavage of foot-and-mouth disease virus polyprotein is mediated by residues located within a 19 amino acid sequence. J. Gen. Virol. 72: (Pt. 112727–32 [Google Scholar]
  140. Salegio EA, Samaranch L, Kells AP, Mittermeyer G, San Sebastian W. 140.  et al. 2013. Axonal transport of adeno-associated viral vectors is serotype-dependent. Gene Ther 20:3348–52 [Google Scholar]
  141. Sando R, Baumgaertel K, Pieraut S, Torabi-Rander N, Wandless TJ. 141.  et al. 2013. Inducible control of gene expression with destabilized Cre. Nat. Methods 10:111085–88 [Google Scholar]
  142. Sauer B, Henderson N. 142.  1988. Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. PNAS 85:145166–70 [Google Scholar]
  143. Saunders A, Johnson CA, Sabatini BL. 143.  2012. Novel recombinant adeno-associated viruses for Cre activated and inactivated transgene expression in neurons. Front. Neural Circuits 6:47 [Google Scholar]
  144. Sayeg MK, Weinberg BH, Cha SS, Goodloe M, Wong WW, Han X. 144.  2015. Rationally designed microRNA-based genetic classifiers target specific neurons in the brain. ACS Synth. Biol. 4:7788–95 [Google Scholar]
  145. Scheer N, Campos-Ortega JA. 145.  1999. Use of the Gal4-UAS technique for targeted gene expression in the zebrafish. Mech. Dev. 80:2153–58 [Google Scholar]
  146. Schroeter EH, Kisslinger JA, Kopan R. 146.  1998. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393:6683382–86 [Google Scholar]
  147. Shikama Y, Hu H, Ohno M, Matsuoka I, Shichishima T, Kimura J. 147.  2010. Transcripts expressed using a bicistronic vector pIREShyg2 are sensitized to nonsense-mediated mRNA decay. BMC Mol. Biol. 11:142 [Google Scholar]
  148. Siegel MS, Isacoff EY. 148.  1997. A genetically encoded optical probe of membrane voltage. Neuron 19:4735–41 [Google Scholar]
  149. Sjulson L, Miesenböck G. 149.  2008. Photocontrol of neural activity: biophysical mechanisms and performance in vivo. Chem. Rev. 108:51588–602 [Google Scholar]
  150. Slimko EM, McKinney S, Anderson DJ, Davidson N, Lester HA. 150.  2002. Selective electrical silencing of mammalian neurons in vitro by the use of invertebrate ligand-gated chloride channels. J. Neurosci. 22:177373–79 [Google Scholar]
  151. Sohal VS, Zhang F, Yizhar O, Deisseroth K. 151.  2009. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459:7247698–702 [Google Scholar]
  152. Spellman T, Rigotti M, Ahmari SE, Fusi S, Gogos JA, Gordon JA. 152.  2015. Hippocampal-prefrontal input supports spatial encoding in working memory. Nature 522:309–14 [Google Scholar]
  153. Spradling AC, Bellen HJ, Hoskins RA. 153.  2011. Drosophila P elements preferentially transpose to replication origins. PNAS 108:3815948–53 [Google Scholar]
  154. Stachniak TJ, Ghosh A, Sternson SM. 154.  2014. Chemogenetic synaptic silencing of neural circuits localizes a hypothalamus→midbrain pathway for feeding behavior. Neuron 82:4797–808 [Google Scholar]
  155. Stamatakis AM, Jennings JH, Ung RL, Blair GA, Weinberg RJ. 155.  et al. 2013. A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron 80:41039–53 [Google Scholar]
  156. Stanley SA, Gagner JE, Damanpour S, Yoshida M, Dordick JS, Friedman JM. 156.  2012. Radio-wave heating of iron oxide nanoparticles can regulate plasma glucose in mice. Science 336:6081604–8 [Google Scholar]
  157. Stanley SA, Sauer J, Kane RS, Dordick JS, Friedman JM. 157.  2015. Remote regulation of glucose homeostasis in mice using genetically encoded nanoparticles. Nat. Med. 21:192–98 [Google Scholar]
  158. Stockinger P, Kvitsiani D, Rotkopf S, Tirian L, Dickson BJ. 158.  2005. Neural circuitry that governs Drosophila male courtship behavior. Cell 121:5795–807 [Google Scholar]
  159. Straub C, Granger AJ, Saulnier JL, Sabatini BL. 159.  2014. CRISPR/Cas9-mediated gene knock-down in post-mitotic neurons. PLOS ONE 9:8e105584 [Google Scholar]
  160. Struhl G, Adachi A. 160.  1998. Nuclear access and action of Notch in vivo. Cell 93:4649–60 [Google Scholar]
  161. Struhl G, Fitzgerald K, Greenwald I. 161.  1993. Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74:2331–45 [Google Scholar]
  162. Stuber GD, Sparta DR, Stamatakis AM, van Leeuwen WA, Hardjoprajitno JE. 162.  et al. 2011. Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475:377–80 [Google Scholar]
  163. Stuber GD, Stamatakis AM, Kantak PA. 163.  2015. Considerations when using Cre-driver rodent lines for studying ventral tegmental area circuitry. Neuron 85:2439–45 [Google Scholar]
  164. Szobota S, Isacoff EY. 164.  2010. Optical control of neuronal activity. Annu. Rev. Biophys. 39:329–48 [Google Scholar]
  165. Tabata H, Nakajima K. 165.  2001. Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103:4865–72 [Google Scholar]
  166. Taniguchi H, He M, Wu P, Kim S, Paik R. 166.  et al. 2011. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71:6995–1013 [Google Scholar]
  167. Tasic B, Menon V, Nguyen TN, Kim TK, Jarsky T. 167.  et al. 2016. Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nat. Neurosci. 19:2335–46 [Google Scholar]
  168. Trichas G, Begbie J, Srinivas S. 168.  2008. Use of the viral 2A peptide for bicistronic expression in transgenic mice. BMC Biol. 6:140 [Google Scholar]
  169. Ugolini G, Kuypers HG, Strick PL. 169.  1989. Transneuronal transfer of herpes virus from peripheral nerves to cortex and brainstem. Science 243:488789–91 [Google Scholar]
  170. Venken KJT, He Y, Hoskins RA, Bellen HJ. 170.  2006. P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314:58061747–51 [Google Scholar]
  171. Waddell S, Armstrong JD, Kitamoto T, Kaiser K, Quinn WG. 171.  2000. The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103:5805–13 [Google Scholar]
  172. Walsh CE, Liu JM, Xiao X, Young NS, Nienhuis AW, Samulski RJ. 172.  1992. Regulated high level expression of a human γ-globin gene introduced into erythroid cells by an adeno-associated virus vector. PNAS 89:157257–61 [Google Scholar]
  173. Wickersham IR, Lyon DC, Barnard RJO, Mori T, Finke S. 173.  et al. 2007. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53:5639–47 [Google Scholar]
  174. Wilson C, Pearson RK, Bellen HJ, O'Kane CJ, Grossniklaus U, Gehring WJ. 174.  1989. P-element–mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes in Drosophila. Genes Dev. 3:91301–13 [Google Scholar]
  175. Witten IB, Steinberg EE, Lee SY, Davidson TJ, Zalocusky KA. 175.  et al. 2011. Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 72:5721–33 [Google Scholar]
  176. Wunderlich FT, Wildner H, Rajewsky K, Edenhofer F. 176.  2001. New variants of inducible Cre recombinase: a novel mutant of Cre-PR fusion protein exhibits enhanced sensitivity and an expanded range of inducibility. Nucleic Acids Res. 29:10E47 [Google Scholar]
  177. Xu R, Janson CG, Mastakov M, Lawlor P, Young D. 177.  et al. 2001. Quantitative comparison of expression with adeno-associated virus (AAV-2) brain-specific gene cassettes. Gene Ther 8:171323–32 [Google Scholar]
  178. Yang XW, Model P, Heintz N. 178.  1997. Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat. Biotechnol. 15:9859–65 [Google Scholar]
  179. Zeisel A, Muñoz-Manchado AB, Codeluppi S, Lönnerberg P, La Manno G. 179.  et al. 2015. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347:62261138–42 [Google Scholar]
  180. Zemanick MC, Strick PL, Dix RD. 180.  1991. Direction of transneuronal transport of herpes simplex virus 1 in the primate motor system is strain-dependent. PNAS 88:188048–51 [Google Scholar]
  181. Zemelman BV, Lee GA, Ng M, Miesenböck G. 181.  2002. Selective photostimulation of genetically chARGed neurons. Neuron 33:115–22 [Google Scholar]
  182. Zemelman BV, Nesnas N, Lee GA, Miesenböck G. 182.  2003. Photochemical gating of heterologous ion channels: remote control over genetically designated populations of neurons. PNAS 100:31352–57 [Google Scholar]
  183. Zervas M, Millet S, Ahn S, Joyner AL. 183.  2004. Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron 43:3345–57 [Google Scholar]
  184. Zirlinger M, Lo L, McMahon J, McMahon AP, Anderson DJ. 184.  2002. Transient expression of the bHLH factor neurogenin-2 marks a subpopulation of neural crest cells biased for a sensory but not a neuronal fate. PNAS 99:128084–89 [Google Scholar]
  185. Zong H, Espinosa JS, Su HH, Muzumdar MD, Luo L. 185.  2005. Mosaic analysis with double markers in mice. Cell 121:3479–92 [Google Scholar]
/content/journals/10.1146/annurev-genet-120215-035011
Loading
/content/journals/10.1146/annurev-genet-120215-035011
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error