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Trans-synaptic Neural Circuit-Tracing with Neurotropic Viruses

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Abstract

A central objective in deciphering the nervous system in health and disease is to define the connections of neurons. The propensity of neurotropic viruses to spread among synaptically-linked neurons makes them ideal for mapping neural circuits. So far, several classes of viral neuronal tracers have become available and provide a powerful toolbox for delineating neural networks. In this paper, we review the recent developments of neurotropic viral tracers and highlight their unique properties in revealing patterns of neuronal connections.

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References

  1. Goodpasture EW, Teague O. Transmission of the Virus of Herpes Febrilis along Nerves in experimentally infected Rabbits. J Med Res 1923, 44: 139–184.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Goodpasture EW. The axis-cylinders of peripheral nerves as protals of entry to the central nervous system for the virus of herpes simplex in experimentally infected rabbits. Am J Pathol 1925, 1: 11–28.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Zhang GR, Zhao H, Abdul-Muneer PM, Cao HY, Li X, Geller AI. Neurons can be labeled with unique hues by helper virus-free HSV-1 vectors expressing Brainbow. J Neurosci Methods 2015, 240: 77–88.

    Article  CAS  PubMed  Google Scholar 

  4. Li B, Zhu L, Zhou Y-C, Guo W-Z, Xu Z-W. Studies on neuronal tracing with pseudorabies virus. Chin J Virol 2014, 30: 333–337.

    Google Scholar 

  5. Kelly RM, Strick PL. Rabies as a transneuronal tracer of circuits in the central nervous system. J Neurosci Methods 2000, 103: 63–71.

    Article  CAS  PubMed  Google Scholar 

  6. Van den Pol AN, Ozduman K, Wollmann G, Ho WSC, Simon I, Yao Y, et al. Viral strategies for studying the brain, including a replication-restricted self-amplifying delta-G vesicular stomatis virus that rapidly expresses transgenes in brain and can generate a multicolor golgi-like expression. J Comp Neurol 2009, 516: 456–481.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Zingg B, Chou XL, Zhang ZG, Mesik L, Liang F, Tao HW, et al. AAV-mediated anterograde transsynaptic tagging: mapping corticocollicular input-defined neural pathways for defense behaviors. Neuron 2017, 93: 33–47.

    Article  CAS  PubMed  Google Scholar 

  8. Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. Analysis of AAV serotypes 1–9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 2008, 16: 1073–1080.

    Article  CAS  PubMed  Google Scholar 

  9. Callaway EM. Transneuronal circuit tracing with neurotropic viruses. Curr Opin Neurobiol 2008, 18: 617–623.

    Article  CAS  PubMed  Google Scholar 

  10. Pomeranz LE, Reynolds AE, Hengartner CJ. Molecular biology of pseudorabies virus: impact on neurovirology and veterinary medicine. Microbiol Mol Biol Rev 2005, 69: 462–500.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Rozenberg F. Herpes simplex encephalitis: pathogenesis and genetic susceptibility. Virologie 2014, 18: 122–135.

    Google Scholar 

  12. Kristensson K, Lycke E, Sjostrand J. Spread of herpes simplex virus in peripheral nerves. Acta Neuropathol 1971, 17: 44–53.

    Article  CAS  PubMed  Google Scholar 

  13. Cook ML, Stevens JG. Pathogenesis of herpetic neuritis and ganglionitis in mice: evidence for intra-axonal transport of infection. Infect Immun 1973, 7: 272–288.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Bak IJ, Markham CH, Cook ML, Stevens JG. Ultrastructural and immunoperoxidase study of striatonigral neurons by means of retrograde axonal transport of herpes simplex virus. Brain Res 1978, 143: 361–368.

    Article  CAS  PubMed  Google Scholar 

  15. Wang YY, Wang Y, Jiang HF, Liu JH, Jia J, Wang K, et al. Impaired glutamatergic projection from the motor cortex to the subthalamic nucleus in 6-hydroxydopamine-lesioned hemi-parkinsonian rats. Exp Neurol 2018, 300: 135–148.

    Article  CAS  PubMed  Google Scholar 

  16. Shimizu N, Doyal MF, Goins WF, Kadekawa K, Wada N, Kanai AJ, et al. Morphological changes in different populations of bladder afferent neurons detected by herpes simplex virus (HSV) vectors with cell-type-specific promoters in mice with spinal cord injury. Neuroscience 2017, 364: 190–201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Zhang GR, Zhao H, Cook N, Svestka M, Choi EM, Jan M, et al. Characteristic and intermingled neocortical circuits encode different visual object discriminations. Behav Brain Res 2017, 331: 261–275.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Senn V, Wolff SB, Herry C, Grenier F, Ehrlich I, Grundemann J, et al. Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron 2014, 81: 428–437.

    Article  CAS  PubMed  Google Scholar 

  19. Sedarati F, Stevens JG. Biological Basis for Virulence of Three Strains of Herpes Simplex Virus Type 1. J Gen Virol 1987, 68: 2389–2395.

    Article  CAS  PubMed  Google Scholar 

  20. Wojaczynski GJ, Engel EA, Steren KE, Enquist LW, Card JP. The neuroinvasive profiles of H129 (herpes simplex virus type 1) recombinants with putative anterograde-only transneuronal spread properties. Brain Struct Funct 2015, 220: 1395–1420.

    Article  CAS  PubMed  Google Scholar 

  21. Ho DY, Mocarski ES. β-galactosidase as a marker in the peripheral and neural tissues of the herpes simplex virus-infected mouse. Virology 1988, 167: 279–283.

    Article  CAS  PubMed  Google Scholar 

  22. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. Green fluorescent protein as a marker for gene-expression. Science 1994, 263: 802–805.

    Article  CAS  PubMed  Google Scholar 

  23. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000, 28: 41–51.

    Article  CAS  PubMed  Google Scholar 

  24. Balan P, Davis-Poynter N, Bell S. An analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoproteins gG gE gI or the putative gJ. J Gen Virol 1994, 75: 1245–1258.

    Article  CAS  PubMed  Google Scholar 

  25. Lilley CE, Groutsi F, Han Z, Palmer JA, Anderson PN, Latchman DS, et al. Multiple immediate-early gene-deficient herpes simplex virus vectors allowing efficient gene delivery to neurons in culture and widespread gene delivery to the central nervous system in vivo. J Virol 2001, 75: 4343–4356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Luo LQ, Callaway EM, Svoboda K. Genetic dissection of neural circuits: a decade of progress. Neuron 2018, 98: 256–281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Dix RD, McKendall RR, Baringer JR. Comparative neurovirulence of herpes simplex virus type 1 strains after peripheral or intracerebral inoculation of BALB/c mice. Infect Immun 1983, 40: 103–112.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Dum RP, Levinthal DJ, Strick PL. The spinothalamic system targets motor and sensory areas in the cerebral cortex of monkeys. J Neurosci 2009, 29: 14223–14235.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. McGovern AE, Davis-Poynter N, Yang SK, Simmons DG, Farrell MJ, Mazzone SB. Evidence for multiple sensory circuits in the brain arising from the respiratory system: an anterograde viral tract tracing study in rodents. Brain Struct Funct 2015, 220: 3683–3699.

    Article  PubMed  Google Scholar 

  30. McGovern AE, Driessen AK, Simmons DG, Powell J, Davis-Poynter N, Farrell MJ, et al. Distinct brainstem and forebrain circuits receiving tracheal sensory neuron inputs revealed using a novel conditional anterograde transsynaptic viral tracing system. J Neurosci 2015, 35: 7041–7055.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ryu V, Watts AG, Xue BZ, Bartness TJ. Bidirectional crosstalk between the sensory and sympathetic motor systems innervating brown and white adipose tissue in male Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 2017, 312: R324–R337.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Rinaman L, Schwartz G. Anterograde transneuronal viral tracing of central viscerosensory pathways in rats. J Neurosci 2004, 24: 2782–2786.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. McGovern AE, Davis-Poynter N, Farrell MJ, Mazzone SB. Transneuronal tracing of airways-related sensory circuitry using herpes simplex virus 1, strain H129. Neuroscience 2012, 207: 148–166.

    Article  CAS  PubMed  Google Scholar 

  34. Lo L, Anderson D. A Cre-dependent, anterograde transsynaptic viral tracer for mapping output pathways of genetically marked neurons. Neuron 2011, 72: 938–950.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Luo L, Callaway EM, Svoboda K. Genetic dissection of neural circuits. Neuron 2008, 57: 634–660.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Dimitrov EL, Yanagawa Y, Usdin TB. Forebrain GABAergic projections to locus coeruleus in mouse. J Comp Neurol 2013, 521: 2373–2397.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Zeng WB, Jiang HF, Gang YD, Song YG, Shen ZZ, Yang H, et al. Anterograde monosynaptic transneuronal tracers derived from herpes simplex virus 1 strain H129. Mol Neurodegener 2017, 12:38: 1–17.

    Google Scholar 

  38. Ugolini G. Advances in viral transneuronal tracing. J Neurosci Methods 2010, 194: 2–20.

    Article  PubMed  Google Scholar 

  39. Brittle EE, Reynolds AE, Enquist LW. Two modes of pseudorabies virus neuroinvasion and lethality in mice. J Virol 2004, 78: 12951–12963.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Platt KB, Mare CJ, Hinz PN. Differentiation of vaecine strains and field isolates of Pseudorabies (Aujeszky’s disease) virus: thermal sensitivity and rabbit virulence markers. Arch Virol 1979, 60: 13–23.

    Article  CAS  PubMed  Google Scholar 

  41. Strack AM, Loewy AD. Pseudorabies virus: a highly specific transneuronal cell body marker in the sympathetic nervous system. J Neurosci 1990, 10: 2139–2147.

    Article  CAS  PubMed  Google Scholar 

  42. Ye C, Zhang QZ, Tian ZJ, Zheng H, Zhao K, Liu F, et al. Genomic characterization of emergent pseudorabies virus in China reveals marked sequence divergence: Evidence for the existence of two major genotypes. Virology 2015, 483: 32–43.

    Article  CAS  PubMed  Google Scholar 

  43. Card JP, Enquist LW. Transneuronal circuit analysis with pseudorabies viruses. Curr Protoc Neurosci 2001, 68: 1–53.

    Google Scholar 

  44. Smith BN, Banfield BW, Smeraski CA, Wilcox CL, Dudek FE, Enquist LW, et al. Pseudorabies virus expressing enhanced green fluorescent protein: A tool for in vitro electrophysiological analysis of transsynaptically labeled neurons in identified central nervous system circuits. Proc Natl Acad Sci U S A 2000, 97: 9264–9269.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Boldogkoi Z, Balint K, Awatramani GB, Balya D, Busskamp V, Viney TJ, et al. Genetically timed, activity-sensor and rainbow transsynaptic viral tools. Nat Methods 2009, 6: 127–130.

    Article  CAS  PubMed  Google Scholar 

  46. DeFalco J, Tomishima M, Liu H, Zhao C, Cai X, Marth JD, et al. Virus-assisted mapping of neural inputs to a feeding center in the hypothalamus. Science 2001, 291: 2608–2613.

    Article  CAS  PubMed  Google Scholar 

  47. Kondoh K, Lu ZH, Ye XL, Olson DP, Lowell BB, Buck LB. A specific area of olfactory cortex involved in stress hormone responses to predator odours. Nature 2016, 532: 103–106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Pomeranz LE, Ekstrand MI, Latcha KN, Smith GA, Enquist LW, Friedman JM. Gene expression profiling with cre-conditional Pseudorabies virus reveals a subset of midbrain neurons that participate in reward circuitry. J Neurosci 2017, 37: 4128–4144.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Livet J, Weissman TA, Kang H, Draft RW, Lu J, Bennis RA, et al. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 2007, 450: 56–62.

    Article  CAS  PubMed  Google Scholar 

  50. Kobiler O, Lipman Y, Therkelsen K, Daubechies I, Enquist LW. Herpesviruses carrying a Brainbow cassette reveal replication and expression of limited numbers of incoming genomes. Nat Commun 2010, 1: 1–8.

    Article  CAS  Google Scholar 

  51. Card JP, Kobiler O, Ludmir EB, Desai V, Sved AF, Enquist LW. A dual infection pseudorabies virus conditional reporter approach to identify projections to collateralized neurons in complex neural circuits. PLoS One 2011, 6: e21141.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Card JP, Kobiler O, McCambridge J, Ebdlahad S, Shan Z, Raizada MK, et al. Microdissection of neural networks by conditional reporter expression from a Brainbow herpesvirus. Proc Natl Acad Sci U S A 2011, 108: 3377–3382.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Strack AM, Sawyer WB, Platt KB, Loewy AD. CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labeling with pseudorabies virus. Brain Res 1989, 491: 274–296.

    Article  CAS  PubMed  Google Scholar 

  54. Kerman IA, Enquist LW, Watson SJ, Yates BJ. Brainstem substrates of sympatho-motor circuitry identified using trans-synaptic tracing with pseudorabies virus recombinants. J Neurosci 2003, 23: 4657–4666.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Krout KE, Mettenleiter TC, Loewy AD. Single CNS neurons link both central motor and cardiosympathetic systems: a double-virus tracing study. Neuroscience 2003, 118: 853–866.

    Article  CAS  PubMed  Google Scholar 

  56. Cano G, Card JP, Sved AF. Dual viral transneuronal tracing of central autonomic circuits involved in the innervation of the two kidneys in rat. J Comp Neurol 2004, 471: 462–481.

    Article  PubMed  Google Scholar 

  57. Kerman IA, Akil H, Watson SJ. Rostral elements of sympatho-motor circuitry: a virally mediated transsynaptic tracing study. J Neurosci 2006, 26: 3423–3433.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Stanley S, Pinto S, Segal J, Perez CA, Viale A, DeFalco J, et al. Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically. Proc Natl Acad Sci U S A 2010, 107: 7024–7029.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Viney TJ, Balint K, Hillier D, Siegert S, Boldogkoi Z, Enquist LW, et al. Local retinal circuits of melanopsin-containing ganglion cells identified by transsynaptic viral tracing. Curr Biol 2007, 17: 981–988.

    Article  CAS  PubMed  Google Scholar 

  60. Billig I, Foris JM, Enquist LW, Card JP, Yates BJ. Definition of neuronal circuitry controlling the activity of phrenic and abdominal motoneurons in the ferret using recombinant strains of pseudorabies virus. J Neurosci 2000, 20: 7446–7454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Yoon H, Enquist LW, Dulac C. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 2005, 123: 669–682.

    Article  CAS  PubMed  Google Scholar 

  62. Luo AH, Tahsili-Fahadan P, Wise RA, Lupica CR, Aston-Jones G. Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science 2011, 333: 353–357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Seiler MJ, Sagdullaev BT, Woch G, Thomas BB, Aramant RB. Transsynaptic virus tracing from host brain to subretinal transplants. Eur J Neurosci 2005, 21: 161–172.

    Article  PubMed  Google Scholar 

  64. Seiler MJ. Retinal transplants restore visual responses: trans-synaptictracing from visually responsive sites labels transplantneurons. Eur J Neurosci 2008, 28: 208–220.

    Article  PubMed  Google Scholar 

  65. Lane MA, White TE, Coutts MA, Jones AL, Sandhu MS, Bloom DC, et al. Cervical prephrenic interneurons in the normal and lesioned spinal cord of the adult rat. J Comp Neurol 2008, 511: 692–709.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Kim JS, Enquist LW, Card JP. Circuit-specific coinfection of neurons in the rat central nervous system with two pseudorabies virus recombinants. J Virol 1999, 73: 9521–9531.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Banfield BW, Kaufman JD, Randall JA, Pickard GE. Development of pseudorabies virus strains expressing red fluorescent proteins: new tools for multisynaptic labeling applications. J Virol 2003, 77: 10106–10112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Ohara S, Inoue K, Yamada M, Yamawaki T, Koganezawa N, Tsutsui K, et al. Dual transneuronal tracing in the rat entorhinal-hippocampal circuit by intracerebral injection of recombinant rabies virus vectors. Front Neuroanat 2009, 3: 1–11.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Ohara S, Inoue K, Witter MP, Iijima T. Untangling neural networks with dual retrograde transsynaptic viral infection. Front Neurosci 2009, 3: 344–349.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Kit S, Kit M, Pirtle EC. Attenuated properties of thymidine kinase-negative deletion mutant of pseudorabies virus. Am J Vet Res 1985, 46: 1359–1367.

    CAS  PubMed  Google Scholar 

  71. Oyibo HK, Znamenskiy P, Oviedo HV, Enquist LW, Zador AM. Long-term Cre-mediated retrograde tagging of neurons using a novel recombinant pseudorabies virus. Front Neuroanat 2014, 8: 86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Wu BW, Engel EA, Enquist LW. Characterization of a replication-incompetent Pseudorabies virus mutant lacking the sole immediate early gene IE180. Mbio 2014, 5: 11.

    Article  CAS  Google Scholar 

  73. Schnell MJ, McGettigan JP, Wirblich C, Papaneri A. The cell biology of rabies virus: using stealth to reach the brain. Nat Rev Microbiol 2010, 8: 51–61.

    Article  CAS  PubMed  Google Scholar 

  74. Dietzschold B, Li J, Faber M, Schnell M. Concepts in the pathogenesis of rabies. Future Virol 2008, 3: 481–490.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Goodpasture EW. A study of rabies, with reference to a neural transmission of the virus in rabbits, and the structure and significance of Negri bodies. Am J Pathol 1925, 1: 547–582.

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Mebatsion T, Konig M, Conzelmann KK. Budding of rabies virus particles in the absence of the spike glycoprotein. Cell 1996, 84: 941–951.

    Article  CAS  PubMed  Google Scholar 

  77. Etessami R, Conzelmann KK, Fadai-Ghotbi B, Natelson B, Tsiang H, Ceccaldi PE. Spread and pathogenic characteristics of a G-deficient rabies virus recombinant: an in vitro and in vivo study. J Gen Virol 2000, 81: 2147–2153.

    Article  CAS  PubMed  Google Scholar 

  78. Wickersham IR, Lyon DC, Barnard RJ, Mori T, Finke S, Conzelmann KK, et al. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 2007, 53: 639–647.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Wall NR, Wickersham IR, Cetin A, De La Parra M, Callaway EM. Monosynaptic circuit tracing in vivo through Cre-dependent targeting and complementation of modified rabies virus. Proc Natl Acad Sci U S A 2010, 107: 21848–21853.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Choi J, Young JA, Callaway EM. Selective viral vector transduction of ErbB4 expressing cortical interneurons in vivo with a viral receptor-ligand bridge protein. Proc Natl Acad Sci U S A 2010, 107: 16703–16708.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Choi J, Callaway EM. Monosynaptic inputs to ErbB4-expressing inhibitory neurons in mouse primary somatosensory cortex. J Comp Neurol 2011, 519: 3402–3414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Osakada F, Callaway EM. Design and generation of recombinant rabies virus vectors. Nat Protoc 2013, 8: 1583–1601.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Marshel JH, Mori T, Nielsen KJ, Callaway EM. Targeting single neuronal networks for gene expression and cell labeling in vivo. Neuron 2010, 67: 562–574.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Stepien AE, Tripodi M, Arber S. Monosynaptic rabies virus reveals premotor network organization and synaptic specificity of cholinergic partition cells. Neuron 2010, 68: 456–472.

    Article  CAS  PubMed  Google Scholar 

  85. Ghanem A, Conzelmann KK. G gene-deficient single-round rabies viruses for neuronal circuit analysis. Virus Res 2016, 216: 41–54.

    Article  CAS  PubMed  Google Scholar 

  86. Kim EJ, Jacobs MW, Ito-Cole T, Callaway EM. Improved monosynaptic neural circuit tracing using engineered rabies virus glycoproteins. Cell Rep 2016, 15: 692–699.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Miyamichi K, Shlomai-Fuchs Y, Shu M, Weissbourd BC, Luo L, Mizrahi A. Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 2013, 80: 1232–1245.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Callaway EM, Luo L. Monosynaptic Circuit Tracing with Glycoprotein-Deleted Rabies Viruses. J Neurosci 2015, 35: 8979–8985.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Miyamichi K, Amat F, Moussavi F, Wang C, Wickersham I, Wall NR, et al. Cortical representations of olfactory input by trans-synaptic tracing. Nature 2011, 472: 191–196.

    Article  CAS  PubMed  Google Scholar 

  90. Arenkiel BR, Hasegawa H, Yi JJ, Larsen RS, Wallace ML, Philpot BD, et al. Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS One 2011, 6: e29423.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Yonehara K, Balint K, Noda M, Nagel G, Bamberg E, Roska B. Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature 2011, 469: 407–410.

    Article  CAS  PubMed  Google Scholar 

  92. Santiago B. Rompani FEM, Adrian Wanner CZ, Chiara N. Roth KY, Roska B. Different modes of visual integration in the lateral geniculate nucleus revealed by single-cell-initiated transsynaptic tracing. Neuron 2017, 93: 767–776.

  93. Vivar C, Potter MC, Choi J, Lee JY, Stringer TP, Callaway EM, et al. Monosynaptic inputs to new neurons in the dentate gyrus. Nat Commun 2012, 3: 1107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Krashes MJ, Shah BP, Madara JC, Olson DP, Strochlic DE, Garfield AS, et al. An excitatory paraventricular nucleus to AgRP neuron circuit that drives hunger. Nature 2014, 507: 238–242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Beier KT, Steinberg EE, DeLoach KE, Xie S, Miyamichi K, Schwarz L, et al. Circuit Architecture of VTA Dopamine Neurons Revealed by Systematic Input-Output Mapping. Cell 2015, 162: 622–634.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Su YT, Gu MY, Chu X, Feng X, Yu YQ. Whole-brain mapping of direct inputs to and axonal projections from GABAergic neurons in the parafacial zone. Neurosci Bull 2018, 34: 485–496.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Garcia I, Huang L, Ung K, Arenkiel BR. Tracing synaptic connectivity onto embryonic stem cell-derived neurons. Stem Cells 2012, 30: 2140–2151.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Schwarz LA, Miyamichi K, Gao XJJ, Beier KT, Weissbourd B, DeLoach KE, et al. Viral-genetic tracing of the input-output organization of a central noradrenaline circuit. Nature 2015, 524: 88–U180.

    Article  CAS  Google Scholar 

  99. Wirblich C, Schnell MJ. Rabies Virus (RV) Glycoprotein expression levels are not critical for pathogenicity of RV. J Virol 2010, 85: 697–704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Mori T, Morimoto K. Rabies virus glycoprotein variants display different patterns in rabies monosynaptic tracing. Front Neuroanat 2014, 7: 47.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Haberl MG, Viana da Silva S, Guest JM, Ginger M, Ghanem A, Mulle C, et al. An anterograde rabies virus vector for high-resolution large-scale reconstruction of 3D neuron morphology. Brain Struct Funct 2015, 220: 1369–1379.

  102. Reardon TR, Murray AJ, Turi GF. Rabies virus CVS-N2c(DG) strain enhances retrograde synaptic transfer and neuronal viability. Neuron 2016, 89: 711–724.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Ciabatti E, Gonzalez-Rueda A, Mariotti L, Morgese F, Tripodi M. Life-Long Genetic and functional access to neural circuits using self-inactivating rabies virus. Cell 2017, 170: 1–17.

    Article  CAS  Google Scholar 

  104. Chatterjee S, Sullivan HA, MacLennan BJ, Xu R, Hou Y, Lavin TK, et al. Nontoxic, double-deletion-mutant rabies viral vectors for retrograde targeting of projection neurons. Nat Neurosci 2018, 21: 638–646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Davidson BL, Breakefield XO. Viral vectors for gene delivery to the nervous system. Nat Rev Neurosci 2003, 4: 353–364.

    Article  CAS  PubMed  Google Scholar 

  106. Roberts A, Buonocore L, Price R, Forman J, Rose JK. Attenuated vesicular stomatitis viruses as vaccine vectors. J Virol 1999, 73: 3723–3732.

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Rodriguez LL. Emergence and re-emergence of vesicular stomatitis in the United States. Virus Res 2002, 85: 211–219.

    Article  CAS  PubMed  Google Scholar 

  108. Lichty BD, Power AT, Stojdl DF, Bell JC. Vesicular stomatitis virus: re-inventing the bullet. Trends Mol Med 2004, 10: 210–216.

    Article  CAS  PubMed  Google Scholar 

  109. Hastie E, Cataldi M, Marriott I, Grdzelishvili VZ. Understanding and altering cell tropism of vesicular stomatitis virus. Virus Res 2013, 176: 16–32.

    Article  CAS  PubMed  Google Scholar 

  110. Beier KT, Saunders AB, Oldenburg IA, Sabatini BL, Cepko CL. Vesicular stomatitis virus with the rabies virus glycoprotein directs retrograde transsynaptic transport among neurons in vivo. Front Neural Circuits 2013, 7: 1–13.

    Article  Google Scholar 

  111. Lundh B. Spread of vesicular stomatitis virus along the visual pathways after retinal infection in the mouse. Acta Neuropathol 1990, 79: 395–401.

    Article  CAS  PubMed  Google Scholar 

  112. Beier KT, Saunders A, Oldenburg IA, Miyamichi K, Akhtar N, Luo L, et al. Anterograde or retrograde transsynaptic labeling of CNS neurons with vesicular stomatitis virus vectors. Proc Natl Acad Sci USA 2011, 108: 15414–15419.

    Article  CAS  PubMed  Google Scholar 

  113. Mundell NA, Beier KT, Pan YA, Lapan SW, Goz Ayturk D, Berezovskii VK, et al. Vesicular stomatitis virus enables gene transfer and transsynaptic tracing in a wide range of organisms. J Comp Neurol 2015, 523: 1639–1663.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Daya S, Berns KI. Gene Therapy using adeno-associated virus vectors. Clin Microbiol Rev 2008, 21: 583–593.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Betley JN, Sternson SM. Adeno-associated viral vectors for mapping, monitoring, and manipulating neural circuits. Hum Gene Ther 2011, 22: 669–677.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Zhao F, Jiang HF, Zeng WB, Shu YS, Luo MH, Duan SM. Anterograde trans-synaptic tagging mediated by adeno-associated virus. Neurosci Bull 2017, 33: 348–350.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This review was supported by the National Natural Science Foundation of China (31671119 and 31871090), the Shenzhen Science and Technology Innovation Commission (JCYJ20160428164440255, JCYJ20170413162938668, JCYJ20170818155056369, and JCYJ20170307170742519), the Shenzhen Discipline Construction Project for Neurobiology (DRCSM [2016]1379), the Japan Society for the Promotion of Science KAKENHI (JP18K08494), and the Japan Science and Technology Agency PRESTO (JPMJPR1784), the Ono Medical Research Foundation, and the Novartis Foundation (Japan) for the Promotion of Science.

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Authors and Affiliations

  1. Guangdong Provincial Key Laboratory of Brain Connectome and Behavior, The Brain Cognition and Brain Disease Institute, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, 518055, China

    Jiamin Li, Taian Liu, Yun Dong & Zhonghua Lu

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Jiamin Li

  3. Division of Endocrinology and Metabolism, Department of Homeostatic Regulation, National Institute for Physiological Sciences, National Institute of Natural Sciences, Myodaiji, Okazaki, Aichi, 444-8585, Japan

    Kunio Kondoh

  4. Japan Science and Technology Agency, PRESTO, Myodaiji, Okazaki, Aichi, 444-8585, Japan

    Kunio Kondoh

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  1. Jiamin Li
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  2. Taian Liu
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  3. Yun Dong
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  4. Kunio Kondoh
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  5. Zhonghua Lu
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Corresponding authors

Correspondence to Kunio Kondoh or Zhonghua Lu.

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Li, J., Liu, T., Dong, Y. et al. Trans-synaptic Neural Circuit-Tracing with Neurotropic Viruses. Neurosci. Bull. 35, 909–920 (2019). https://doi.org/10.1007/s12264-019-00374-9

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  • DOI: https://doi.org/10.1007/s12264-019-00374-9

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