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THE NEED OF COMPUTATIONAL METHODS

SEROTONERGIC NEURONS DIRECTLY CONTROL IMPULSIVE BEHAVIORS IN RATS

5 DISSCUSSION & PERSPECTIVES

5.3 THE NEED OF COMPUTATIONAL METHODS

The study of neuroanatomy involves highly labor-intensive work, including sectioning, staining, imagine, and data analysis. With the emergence of global collaborative brain projects such as the BRAIN Initiative, more and more high-throughput data have been produced. Therefore the urge of powerful computational tools been implemented into every aspect of neuroscience studies is in strong need. Our second paper is trying to make such an attempt. Moreover, better computational methods are needed for combining high-throughput neuroanatomy data with other high-throughput techniques (e.g., single cell sequencing).

6 ACKNOWLEDGEMENTS

There are many people I would like to thank for supporting me through all these years in Sweden. First of all, thank my main supervisor Marie Carlén for taking me as a PhD student and all your scientific guidance over the years. I really appreciated the open atmosphere in the lab and all the freedom in research. Thank you for showing me how to put everything together and make things happen. I’d also like to thank Dinos Meletis, my co-supervisor, who actually introduced me into the rabies world. Thank you for the guidance and discussions about virus.

Thank all my collaborators for adding your expertise to the projects in this thesis: Sofie Ährlund- Richter, Daniel Fürth, Hoseok Kim, Xinming Wang, Iskra Pollak Dorocic, Felix Wahl, Yvonne Johansson, Laura Pozzi, Gilad Silberberg, Daniel Kaping, Marc Parent, Ourania Tzortzi, Antje Märtin, Iakovos Lazaridis, Giada Spigolon, and Gilberto Fisone.

Thank you to all the previous and present DMC members for both the support in work and life, for the beers and retreats. Special thanks to: Sofie, for being always positive and keeping driving the project together; Xinming, for being always supportive to each other and all those brilliant molecular ideas; Hoseok, for all the kpop, Asian food and culture discussions, and all the hours we spent together in the animal house; Rania and Antje for the accompany in all those unforgettable working evenings and weekends; Daniel for amazing virus ideas; Iskra for working together and making it happen; Calvin for introducing me to the ephys world and fruitful discussions about science; Nicolas for knowing China better than me and all the sports/movie/food; Moritz for tlhingan and video game discussion; Josie for traveling together in Crete; Cantin for communism and beers; Micke for all the hours spent in the virus room and choir discussions.

Thank all my friends in the department and KI: the Hermanssons (Esra, Giulia, Xiaofei, Kuba, Michalina, and Aileen) for always being fun; Yvonne for doing gym together; Maya, Caro, Maria for the parties and beers; the Chinese lunch crew: Du Kai and Song Jianren for all the scientific and life discussions; Qian Yu for being as a doraemon; Jiang Shan for sharing running experiences; Li- ju for being as a strong girl; Yongtao for all the positive energy; Haohao and Yiqiao for random chats; Jian Yan for being my role model as a scientist; Jia Ting for showing me how hard-working a person can be; Yimeng and Bei Wei for showing me how to be doing great science yet still be nice; Minghui He for having lunch now and then and being updated with information from old colleagues; Rui Wang for the Swedish studies together and being by my side; Juan Du for showing me how energetic a new PI can be.

Thank you to all my Chinese friends here in Stockholm. Special thanks to: Ci Song for being the other me and taking care of me for so many years; Simba Qiu for being always by my side, giving me great advices, pushing me out of my comfort zone and picking up my emotional breaking down phone calls; my Stockholm Kinesiska Kör friends: Minyue Li for being always positive; Molan Li for also being as my sports buddy; Meiying Sun for all the wonderful food and games; Siyang Leo Dai, Jidong Tan, Ying Liu, Jisheng Wang, Jenny Huang, Xiaodong Zou, Hongmei Yan and Yaping Qu for being working and having fun together for the choir and being as friends; my poker game friends: Qiongzi for being generous and positive; Zheng Chang for taking care of Ci; Qiang Zhang, Yuning, Huan, Yixin for having fun together every Friday; Suo Chen for all the ballet shows together; my badminton friends: Yayun Feng for all the food, wine and game nights; Tianwei Gu for making me love Nanjing more; Chenglin for your hujian accent; Xu Hao for being my badminton double-mix partner; Yuncheng Wang for also playing with twitch; Lidi Xu, Peng Zhang, Jiangnan Luo, Genping, Hongyan, Fu Ping, Hu Wei, Zhang Qiong and Xiao Wei for organizing and sharing all the great moments together; my gym and board game friends: Xie Meng and Liu Yilin for gym, jokes and drinking talks; my barbeque friends: Yue Wang for cooking and ice-skating demonstrations; An Qin for being an inspiring drone pilot/engineer/coder/tailor/cook; Sheng Mugua Zhang for being the most memeda person; Gao Peng and Zhou Yuan for lappis garden treats; Yutong, Wenwen and

Yang Ke for dog talks; Xia Zhe for the shanghai homemade food treats; Hongyi for showing the robots; Qiuchen for exchanging stuff; Zhifei He for having the same sanguan; Ouyang Zhan for sharing running experience; Amir and Xi for being great neighbors.

Thank you to all my life long friends outside Sweden. Special thanks to: Phyllis Zhang, for always being full of energy and pushing me moving forward; Yisheng Wu, for all the support and phone calls over the years, and all the realistic suggestions; Zi Li, for staying idealist; Huajia Wang, for all the Chinese indie music and great ideas we’ve shared; Wei Lai, for the volleyball talks and showing me the royal botany garden; Sun Pei and Xuefan, for traveling together in Europe; Fangyan, for all the great German Chinese food; Felix Wong for volleyball and career-path discussions; Du Xin and Yan Qiang for being super generous and encouraging; Yinan Gong, for showing me how to stay calm and fight for yourself.

Thank you to my parents: Yongjian Xuan宣永健and Xingxin Xu许星⼼.

感谢爸爸妈妈多年来对我的教育,⼀路上的爱和⽆条件的支持。正因为有你们,我才 可以直直的往前⾛。爸爸的乐观开朗, 妈妈的⾏事果断,让我受益良多。

我还想说的是,⼀路⾛来并没有想象中的容易,谢谢⼤家陪我⼀起经历和成长。 不念过往,不畏将来,不忘初⼼。

7 REFERENCES

Akerboom, J., Chen, T.W., Wardill, T.J., Tian, L., Marvin, J.S., Mutlu, S., Calderon, N.C., Esposti, F., Borghuis, B.G., Sun, X.R., Gordus, A., Orger, M.B., Portugues, R., Engert, F., Macklin, J.J., Filosa, A., Aggarwal, A., Kerr, R.A., Takagi, R., Kracun, S., Shigetomi, E., Khakh, B.S., Baier, H., Lagnado, L., Wang, S.S., Bargmann, C.I., Kimmel, B.E., Jayaraman, V., Svoboda, K., Kim, D.S., Schreiter, E.R. & Looger, L.L. (2012) Optimization of a GCaMP calcium indicator for neural activity imaging.

J Neurosci, 32, 13819-13840.

Albertini, A.A., Baquero, E., Ferlin, A. & Gaudin, Y. (2012) Molecular and cellular aspects of rhabdovirus entry. Viruses, 4, 117-139.

Albisetti, G.W., Ghanem, A., Foster, E., Conzelmann, K.K., Zeilhofer, H.U. & Wildner, H. (2017) Identification of Two Classes of Somatosensory Neurons That Display Resistance to Retrograde Infection by Rabies Virus. J Neurosci, 37, 10358-10371.

Andermann, M.L., Gilfoy, N.B., Goldey, G.J., Sachdev, R.N., Wolfel, M., McCormick, D.A., Reid, R.C. & Levene, M.J. (2013) Chronic cellular imaging of entire cortical columns in awake mice using microprisms. Neuron, 80, 900-913.

Baer, G.M. (1991) The natural history of rabies. CRC press.

Bechara, A., Laumonnerie, C., Vilain, N., Kratochwil, C.F., Cankovic, V., Maiorano, N.A., Kirschmann, M.A., Ducret, S. & Rijli, F.M. (2015) Hoxa2 Selects Barrelette Neuron Identity and Connectivity in the Mouse Somatosensory Brainstem. Cell reports, 13, 783-797.

Beier, K.T., Kim, C.K., Hoerbelt, P., Hung, L.W., Heifets, B.D., DeLoach, K.E., Mosca, T.J., Neuner, S., Deisseroth, K., Luo, L. & Malenka, R.C. (2017) Rabies screen reveals GPe control of cocaine-triggered plasticity. Nature, 549, 345-350.

Beier, K.T., Saunders, A., Oldenburg, I.A., Miyamichi, K., Akhtar, N., Luo, L., Whelan, S.P., Sabatini, B. & Cepko, C.L. (2011) Anterograde or retrograde transsynaptic labeling of CNS neurons with vesicular stomatitis virus vectors. Proceedings of the National

Berndt, A., Lee, S.Y., Ramakrishnan, C. & Deisseroth, K. (2014) Structure-guided

transformation of channelrhodopsin into a light-activated chloride channel. Science,

344, 420-424.

Bizot, J., Le Bihan, C., Puech, A.J., Hamon, M. & Thiebot, M. (1999) Serotonin and tolerance to delay of reward in rats. Psychopharmacology (Berl), 146, 400-412.

Bohland, J.W., Wu, C., Barbas, H., Bokil, H., Bota, M., Breiter, H.C., Cline, H.T., Doyle, J.C., Freed, P.J., Greenspan, R.J., Haber, S.N., Hawrylycz, M., Herrera, D.G.,

Hilgetag, C.C., Huang, Z.J., Jones, A., Jones, E.G., Karten, H.J., Kleinfeld, D., Kotter, R., Lester, H.A., Lin, J.M., Mensh, B.D., Mikula, S., Panksepp, J., Price, J.L.,

Safdieh, J., Saper, C.B., Schiff, N.D., Schmahmann, J.D., Stillman, B.W., Svoboda, K., Swanson, L.W., Toga, A.W., Van Essen, D.C., Watson, J.D. & Mitra, P.P. (2009) A proposal for a coordinated effort for the determination of brainwide

neuroanatomical connectivity in model organisms at a mesoscopic scale. PLoS

Comput Biol, 5, e1000334.

Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. (2005) Millisecond- timescale, genetically targeted optical control of neural activity. Nat Neurosci, 8, 1263-1268.

Buehr, M., Meek, S., Blair, K., Yang, J., Ure, J., Silva, J., McLay, R., Hall, J., Ying, Q.L. & Smith, A. (2008) Capture of authentic embryonic stem cells from rat blastocysts. Cell,

135, 1287-1298.

Butt, S.J., Fuccillo, M., Nery, S., Noctor, S., Kriegstein, A., Corbin, J.G. & Fishell, G. (2005) The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron, 48, 591-604.

Carlen, M. (2017) What constitutes the prefrontal cortex? Science, 358, 478-482.

Chatterjee, S., Sullivan, H.A., MacLennan, B.J., Xu, R., Hou, Y., Lavin, T.K., Lea, N.E., Michalski, J.E., Babcock, K.R., Dietrich, S., Matthews, G.A., Beyeler, A., Calhoon, G.G., Glober, G., Whitesell, J.D., Yao, S., Cetin, A., Harris, J.A., Zeng, H., Tye, K.M., Reid, R.C. & Wickersham, I.R. (2018) Nontoxic, double-deletion-mutant rabies viral vectors for retrograde targeting of projection neurons. Nat Neurosci.

Chen, T.W., Wardill, T.J., Sun, Y., Pulver, S.R., Renninger, S.L., Baohan, A., Schreiter, E.R., Kerr, R.A., Orger, M.B., Jayaraman, V., Looger, L.L., Svoboda, K. & Kim, D.S.

(2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature, 499, 295-300.

Ciabatti, E., Gonzalez-Rueda, A., Mariotti, L., Morgese, F. & Tripodi, M. (2017) Life-Long Genetic and Functional Access to Neural Circuits Using Self-Inactivating Rabies Virus. Cell, 170, 382-392 e314.

Cui, X., Ji, D., Fisher, D.A., Wu, Y., Briner, D.M. & Weinstein, E.J. (2011) Targeted

integration in rat and mouse embryos with zinc-finger nucleases. Nat Biotechnol, 29, 64-67.

Dahlstrom, A. & Fuxe, K. (1964) Localization of monoamines in the lower brain stem.

Experientia, 20, 398-399.

Dalley, J.W. & Roiser, J.P. (2012) Dopamine, serotonin and impulsivity. Neuroscience, 215, 42-58.

Dana, H., Mohar, B., Sun, Y., Narayan, S., Gordus, A., Hasseman, J.P., Tsegaye, G., Holt, G.T., Hu, A., Walpita, D., Patel, R., Macklin, J.J., Bargmann, C.I., Ahrens, M.B., Schreiter, E.R., Jayaraman, V., Looger, L.L., Svoboda, K. & Kim, D.S. (2016) Sensitive red protein calcium indicators for imaging neural activity. Elife, 5.

DeNardo, L.A., Berns, D.S., DeLoach, K. & Luo, L. (2015a) Connectivity of mouse somatosensory and prefrontal cortex examined with trans-synaptic tracing. Nat

Neurosci, 18, 1687-1697.

DeNardo, L.A., Berns, D.S., DeLoach, K. & Luo, L. (2015b) Connectivity of mouse somatosensory and prefrontal cortex examined with trans-synaptic tracing. Nat

Neurosci, 18, 1687-1697.

Dombeck, D.A., Khabbaz, A.N., Collman, F., Adelman, T.L. & Tank, D.W. (2007) Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron, 56, 43-57.

Donoghue, J.P. & Herkenham, M. (1986) Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res,

Erspamer, V. & Asero, B. (1952) Identification of enteramine, the specific hormone of the enterochromaffin cell system, as 5-hydroxytryptamine. Nature, 169, 800-801.

Etessami, R., Conzelmann, K.K., Fadai-Ghotbi, B., Natelson, B., Tsiang, H. & Ceccaldi, P.E. (2000) Spread and pathogenic characteristics of a G-deficient rabies virus

recombinant: an in vitro and in vivo study. J Gen Virol, 81, 2147-2153.

Fenno, L.E., Mattis, J., Ramakrishnan, C., Hyun, M., Lee, S.Y., He, M., Tucciarone, J., Selimbeyoglu, A., Berndt, A., Grosenick, L., Zalocusky, K.A., Bernstein, H.,

Swanson, H., Perry, C., Diester, I., Boyce, F.M., Bass, C.E., Neve, R., Huang, Z.J. & Deisseroth, K. (2014) Targeting cells with single vectors using multiple-feature Boolean logic. Nat Methods, 11, 763-772.

Finke, S. & Conzelmann, K.K. (2005) Replication strategies of rabies virus. Virus Res, 111, 120-131.

Fogarty, M., Grist, M., Gelman, D., Marin, O., Pachnis, V. & Kessaris, N. (2007) Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J Neurosci, 27, 10935-10946.

Gerfen, C.R. & Sawchenko, P.E. (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals:

immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res, 290, 219-238.

Geurts, A.M., Cost, G.J., Freyvert, Y., Zeitler, B., Miller, J.C., Choi, V.M., Jenkins, S.S., Wood, A., Cui, X., Meng, X., Vincent, A., Lam, S., Michalkiewicz, M., Schilling, R., Foeckler, J., Kalloway, S., Weiler, H., Menoret, S., Anegon, I., Davis, G.D., Zhang, L., Rebar, E.J., Gregory, P.D., Urnov, F.D., Jacob, H.J. & Buelow, R. (2009)

Knockout rats via embryo microinjection of zinc-finger nucleases. Science, 325, 433.

Ghosh, K.K., Burns, L.D., Cocker, E.D., Nimmerjahn, A., Ziv, Y., Gamal, A.E. & Schnitzer, M.J. (2011) Miniaturized integration of a fluorescence microscope. Nat Methods, 8, 871-878.

Gonatas, N.K. (1979) The use of lectins and cholera toxin for the detection of surface carbohydrates of cultured neurons and neuroblastoma. J Histochem Cytochem, 27, 1165-1166.

Gong, S., Doughty, M., Harbaugh, C.R., Cummins, A., Hatten, M.E., Heintz, N. & Gerfen, C.R. (2007) Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J Neurosci, 27, 9817-9823.

Gong, S., Zheng, C., Doughty, M.L., Losos, K., Didkovsky, N., Schambra, U.B., Nowak, N.J., Joyner, A., Leblanc, G., Hatten, M.E. & Heintz, N. (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature,

425, 917-925.

Haubensak, W., Kunwar, P.S., Cai, H., Ciocchi, S., Wall, N.R., Ponnusamy, R., Biag, J., Dong, H.W., Deisseroth, K., Callaway, E.M., Fanselow, M.S., Luthi, A. & Anderson, D.J. (2010) Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature, 468, 270-276.

Hoover, W.B. & Vertes, R.P. (2007) Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct, 212, 149-179.

Hunnicutt, B.J., Long, B.R., Kusefoglu, D., Gertz, K.J., Zhong, H. & Mao, T. (2014) A comprehensive thalamocortical projection map at the mesoscopic level. Nat Neurosci,

17, 1276-1285.

Jennings, J.H., Ung, R.L., Resendez, S.L., Stamatakis, A.M., Taylor, J.G., Huang, J., Veleta, K., Kantak, P.A., Aita, M., Shilling-Scrivo, K., Ramakrishnan, C., Deisseroth, K., Otte, S. & Stuber, G.D. (2015) Visualizing hypothalamic network dynamics for appetitive and consummatory behaviors. Cell, 160, 516-527.

Jercog, P., Rogerson, T. & Schnitzer, M.J. (2016) Large-Scale Fluorescence Calcium- Imaging Methods for Studies of Long-Term Memory in Behaving Mammals. Cold

Spring Harb Perspect Biol, 8.

Jiang, X., Shen, S., Cadwell, C.R., Berens, P., Sinz, F., Ecker, A.S., Patel, S. & Tolias, A.S. (2015) Principles of connectivity among morphologically defined cell types in adult neocortex. Science, 350, aac9462.

Jung, J.C., Mehta, A.D., Aksay, E., Stepnoski, R. & Schnitzer, M.J. (2004) In vivo

mammalian brain imaging using one- and two-photon fluorescence microendoscopy.

J Neurophysiol, 92, 3121-3133.

Kim, C.K., Yang, S.J., Pichamoorthy, N., Young, N.P., Kauvar, I., Jennings, J.H., Lerner, T.N., Berndt, A., Lee, S.Y., Ramakrishnan, C., Davidson, T.J., Inoue, M., Bito, H. &

Deisseroth, K. (2016a) Simultaneous fast measurement of circuit dynamics at multiple sites across the mammalian brain. Nat Methods, 13, 325-328.

Kim, E.J., Jacobs, M.W., Ito-Cole, T. & Callaway, E.M. (2016b) Improved Monosynaptic Neural Circuit Tracing Using Engineered Rabies Virus Glycoproteins. Cell reports,

15, 692-699.

Kim, Y., Venkataraju, K.U., Pradhan, K., Mende, C., Taranda, J., Turaga, S.C., Arganda- Carreras, I., Ng, L., Hawrylycz, M.J., Rockland, K.S., Seung, H.S. & Osten, P. (2015) Mapping social behavior-induced brain activation at cellular resolution in the mouse.

Cell reports, 10, 292-305.

King, M.A., Louis, P.M., Hunter, B.E. & Walker, D.W. (1989) Biocytin: a versatile anterograde neuroanatomical tract-tracing alternative. Brain Res, 497, 361-367.

Klapoetke, N.C., Murata, Y., Kim, S.S., Pulver, S.R., Birdsey-Benson, A., Cho, Y.K., Morimoto, T.K., Chuong, A.S., Carpenter, E.J., Tian, Z., Wang, J., Xie, Y., Yan, Z., Zhang, Y., Chow, B.Y., Surek, B., Melkonian, M., Jayaraman, V., Constantine-Paton, M., Wong, G.K. & Boyden, E.S. (2014) Independent optical excitation of distinct neural populations. Nat Methods, 11, 338-346.

Kobbert, C., Apps, R., Bechmann, I., Lanciego, J.L., Mey, J. & Thanos, S. (2000) Current concepts in neuroanatomical tracing. Prog Neurobiol, 62, 327-351.

Kristensson, K. & Olsson, Y. (1971) Retrograde axonal transport of protein. Brain Res, 29, 363-365.

Kvitsiani, D., Ranade, S., Hangya, B., Taniguchi, H., Huang, J.Z. & Kepecs, A. (2013) Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. Nature, 498, 363-366.

Lecoq, J., Savall, J., Vucinic, D., Grewe, B.F., Kim, H., Li, J.Z., Kitch, L.J. & Schnitzer, M.J. (2014) Visualizing mammalian brain area interactions by dual-axis two-photon calcium imaging. Nat Neurosci, 17, 1825-1829.

Lee, S., Hjerling-Leffler, J., Zagha, E., Fishell, G. & Rudy, B. (2010) The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J Neurosci, 30, 16796-16808.

Lentz, T.L., Burrage, T.G., Smith, A.L., Crick, J. & Tignor, G.H. (1982) Is the acetylcholine receptor a rabies virus receptor? Science, 215, 182-184.

Lerner, T.N., Shilyansky, C., Davidson, T.J., Evans, K.E., Beier, K.T., Zalocusky, K.A., Crow, A.K., Malenka, R.C., Luo, L., Tomer, R. & Deisseroth, K. (2015) Intact-Brain Analyses Reveal Distinct Information Carried by SNc Dopamine Subcircuits. Cell,

162, 635-647.

Li, P., Tong, C., Mehrian-Shai, R., Jia, L., Wu, N., Yan, Y., Maxson, R.E., Schulze, E.N., Song, H., Hsieh, C.L., Pera, M.F. & Ying, Q.L. (2008) Germline competent embryonic stem cells derived from rat blastocysts. Cell, 135, 1299-1310.

London, T.D., Licholai, J.A., Szczot, I., Ali, M.A., LeBlanc, K.H., Fobbs, W.C. & Kravitz, A.V. (2018) Coordinated ramping of dorsal striatal pathways preceding food approach and consumption. J Neurosci.

Low, R.J., Gu, Y. & Tank, D.W. (2014) Cellular resolution optical access to brain regions in fissures: imaging medial prefrontal cortex and grid cells in entorhinal cortex.

Proceedings of the National Academy of Sciences of the United States of America,

111, 18739-18744.

Lutcke, H., Murayama, M., Hahn, T., Margolis, D.J., Astori, S., Zum Alten Borgloh, S.M., Gobel, W., Yang, Y., Tang, W., Kugler, S., Sprengel, R., Nagai, T., Miyawaki, A., Larkum, M.E., Helmchen, F. & Hasan, M.T. (2010) Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice. Front Neural Circuits, 4, 9.

Ma, Y., Ma, J., Zhang, X., Chen, W., Yu, L., Lu, Y., Bai, L., Shen, B., Huang, X. & Zhang, L. (2014) Generation of eGFP and Cre knockin rats by CRISPR/Cas9. FEBS J, 281, 3779-3790.

Madisen, L., Zwingman, T.A., Sunkin, S.M., Oh, S.W., Zariwala, H.A., Gu, H., Ng, L.L., Palmiter, R.D., Hawrylycz, M.J., Jones, A.R., Lein, E.S. & Zeng, H. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci, 13, 133-140.

Matsuyama, M., Ohashi, Y., Tsubota, T., Yaguchi, M., Kato, S., Kobayashi, K. & Miyashita, Y. (2015) Avian sarcoma leukosis virus receptor-envelope system for simultaneous dissection of multiple neural circuits in mammalian brain. Proceedings of the

Mebatsion, T., Konig, M. & Conzelmann, K.K. (1996) Budding of rabies virus particles in the absence of the spike glycoprotein. Cell, 84, 941-951.

Mi, D., Li, Z., Lim, L., Li, M., Moissidis, M., Yang, Y., Gao, T., Hu, T.X., Pratt, T., Price, D.J., Sestan, N. & Marin, O. (2018) Early emergence of cortical interneuron diversity in the mouse embryo. Science.

Miyamichi, K., Amat, F., Moussavi, F., Wang, C., Wickersham, I., Wall, N.R., Taniguchi, H., Tasic, B., Huang, Z.J., He, Z., Callaway, E.M., Horowitz, M.A. & Luo, L. (2011) Cortical representations of olfactory input by trans-synaptic tracing. Nature, 472, 191- 196.

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

Miyazaki, K., Miyazaki, K.W. & Doya, K. (2012) The role of serotonin in the regulation of patience and impulsivity. Mol Neurobiol, 45, 213-224.

Nagel, G., Ollig, D., Fuhrmann, M., Kateriya, S., Musti, A.M., Bamberg, E. & Hegemann, P. (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science, 296, 2395-2398.

Nakai, J., Ohkura, M. & Imoto, K. (2001) A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol, 19, 137-141.

Oh, S.W., Harris, J.A., Ng, L., Winslow, B., Cain, N., Mihalas, S., Wang, Q., Lau, C., Kuan, L., Henry, A.M., Mortrud, M.T., Ouellette, B., Nguyen, T.N., Sorensen, S.A.,

Slaughterbeck, C.R., Wakeman, W., Li, Y., Feng, D., Ho, A., Nicholas, E., Hirokawa, K.E., Bohn, P., Joines, K.M., Peng, H., Hawrylycz, M.J., Phillips, J.W., Hohmann, J.G., Wohnoutka, P., Gerfen, C.R., Koch, C., Bernard, A., Dang, C., Jones, A.R. & Zeng, H. (2014) A mesoscale connectome of the mouse brain. Nature, 508, 207-214.

Osakada, Y. & Cui, B. (2011) Real-time visualization of axonal transport in neurons.

Methods Mol Biol, 670, 231-243.

Petreanu, L., Gutnisky, D.A., Huber, D., Xu, N.L., O'Connor, D.H., Tian, L., Looger, L. & Svoboda, K. (2012) Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature, 489, 299-303.

Reardon, T.R., Murray, A.J., Turi, G.F., Wirblich, C., Croce, K.R., Schnell, M.J., Jessell, T.M. & Losonczy, A. (2016) Rabies Virus CVS-N2c(DeltaG) Strain Enhances Retrograde Synaptic Transfer and Neuronal Viability. Neuron, 89, 711-724.

Renier, N., Adams, E.L., Kirst, C., Wu, Z., Azevedo, R., Kohl, J., Autry, A.E., Kadiri, L., Umadevi Venkataraju, K., Zhou, Y., Wang, V.X., Tang, C.Y., Olsen, O., Dulac, C., Osten, P. & Tessier-Lavigne, M. (2016) Mapping of Brain Activity by Automated Volume Analysis of Immediate Early Genes. Cell, 165, 1789-1802.

Roche, S., Bressanelli, S., Rey, F.A. & Gaudin, Y. (2006) Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science, 313, 187-191.

Roche, S., Rey, F.A., Gaudin, Y. & Bressanelli, S. (2007) Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science, 315, 843-848.

Rose, J.E. & Woolsey, C.N. (1948) The orbitofrontal cortex and its connections with the mediodorsal nucleus in rabbit, sheep and cat. Res Publ Assoc Res Nerv Ment Dis, 27

(1 vol.), 210-232.

Schulz, K., Sydekum, E., Krueppel, R., Engelbrecht, C.J., Schlegel, F., Schroter, A., Rudin, M. & Helmchen, F. (2012) Simultaneous BOLD fMRI and fiber-optic calcium recording in rat neocortex. Nat Methods, 9, 597-602.

Schwab, M.E. & Agid, I. (1979) Labelled wheat germ agglutinin and tetanus toxin as highly sensitive retrograde tracers in the CNS: the afferent fiber connections of the rat nucleus caudatus. Int J Neurol, 13, 117-126.

Seidler, B., Schmidt, A., Mayr, U., Nakhai, H., Schmid, R.M., Schneider, G. & Saur, D. (2008) A Cre-loxP-based mouse model for conditional somatic gene expression and knockdown in vivo by using avian retroviral vectors. Proceedings of the National

Academy of Sciences of the United States of America, 105, 10137-10142.

Sesack, S.R., Deutch, A.Y., Roth, R.H. & Bunney, B.S. (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol, 290, 213- 242.

Sissoeff, L., Mousli, M., England, P. & Tuffereau, C. (2005) Stable trimerization of

recombinant rabies virus glycoprotein ectodomain is required for interaction with the

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