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Viral-genetic tracing of the input-output organization of a central noradrenaline circuit
Open accessAbstract
Deciphering how neural circuits are anatomically organized with regard to input and output is instrumental in understanding how the brain processes information. For example, locus coeruleus noradrenaline (also known as norepinephrine) (LC-NE) neurons receive input from and send output to broad regions of the brain and spinal cord, and regulate diverse functions including arousal, attention, mood and sensory gating. However, it is unclear how LC-NE neurons divide up their brain-wide projection patterns and whether different LC-NE neurons receive differential input. Here we developed a set of viral-genetic tools to quantitatively analyse the input-output relationship of neural circuits, and applied these tools to dissect the LC-NE circuit in mice. Rabies-virus-based input mapping indicated that LC-NE neurons receive convergent synaptic input from many regions previously identified as sending axons to the locus coeruleus, as well as from newly identified presynaptic partners, including cerebellar Purkinje cells. The 'tracing the relationship between input and output' method (or TRIO method) enables trans-synaptic input tracing from specific subsets of neurons based on their projection and cell type. We found that LC-NE neurons projecting to diverse output regions receive mostly similar input. Projection-based viral labelling revealed that LC-NE neurons projecting to one output region also project to all brain regions we examined. Thus, the LC-NE circuit overall integrates information from, and broadcasts to, many brain regions, consistent with its primary role in regulating brain states. At the same time, we uncovered several levels of specificity in certain LC-NE sub-circuits. These tools for mapping output architecture and input-output relationship are applicable to other neuronal circuits and organisms. More broadly, our viral-genetic approaches provide an efficient intersectional means to target neuronal populations based on cell type and projection pattern.
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“Thus, the input-output architecture of the DR serotonin system differs from that of the locus coeruleus norepinephrine system with more homogeneous input and output (Schwarz et al., 2015), and resembles more closely those of the midbrain dopamine systems (Beier et al., 2015; Lerner et al., 2015), with biased input and segregated output.”
From Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems (2018) · cites this paper as Schwarz et al., 2015
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Cites
A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
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., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907
Dahlstroem, A., & Fuxé, K. (1964) · PubMed · Cited by 5,133
Aston-Jones, G., & Bloom, F. (1981) · The Journal of Neuroscience · doi:10.1523/jneurosci.01-08-00876.1981 · Cited by 1,960
Swanson, L. W., & Hartman, B. K. (1975) · The Journal of Comparative Neurology · doi:10.1002/cne.901630406 · Cited by 1,475
Whole-Brain Mapping of Direct Inputs to Midbrain Dopamine Neurons
Watabe‐Uchida, M., Zhu, L., Ogawa, S. K., Vamanrao, A., & Uchida, N. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.017 · Cited by 1,277
Monosynaptic Restriction of Transsynaptic Tracing from Single, Genetically Targeted Neurons
Wickersham, I. R., Lyon, D. C., Barnard, R. J. O., Mori, T., Finke, S., Conzelmann, K., Young, J. A. T., & Callaway, E. M. (2007) · Neuron · doi:10.1016/j.neuron.2007.01.033 · Cited by 1,176
Orienting and reorienting: the locus coeruleus mediates cognition through arousal
Sara, S. J., & Bouret, S. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.011 · Cited by 1,056
Tuning arousal with optogenetic modulation of locus coeruleus neurons
Carter, M. E., Yizhar, O., Chikahisa, S., Nguyen, H., Adamantidis, A., Nishino, S., Deisseroth, K., & de Lecea, L. (2010) · Nature Neuroscience · doi:10.1038/nn.2682 · Cited by 993
Gong, S., Doughty, M., Harbaugh, C. R., Cummins, A., Hatten, M. E., Heintz, N., & Gerfen, C. R. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2707-07.2007 · Cited by 977
Genetic Dissection of Neural Circuits
Luo, L., Callaway, E. M., & Svoboda, K. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.002 · Cited by 771
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Chan, K. Y., Jang, M. J., Yoo, B. B., Greenbaum, A., Ravi, N., Wu, W.-L., Sánchez-Guardado, L., Lois, C., Mazmanian, S. K., Deverman, B. E., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4593 · Cited by 1,578
Joshi, S., Li, Y., Kalwani, R. M., & Gold, J. I. (2016) · Neuron · doi:10.1016/j.neuron.2015.11.028 · Cited by 1,387
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Surmeier, D. J., Obeso, J. A., & Halliday, G. M. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.178 · Cited by 1,116
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Beier, K. T., Steinberg, E. E., DeLoach, K. E., Xie, S., Miyamichi, K., Schwarz, L., Gao, X. J., Kremer, E. J., Malenka, R. C., & Luo, L. (2015) · Cell · doi:10.1016/j.cell.2015.07.015 · Cited by 1,068
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Scammell, T. E., Arrigoni, E., & Lipton, J. O. (2017) · Neuron · doi:10.1016/j.neuron.2017.01.014 · Cited by 966
Locus coeruleus and dopaminergic consolidation of everyday memory
Takeuchi, T., Duszkiewicz, A. J., Sonneborn, A., Spooner, P. A., Yamasaki, M., Watanabe, M., Smith, C. C., Fernández, G., Deisseroth, K., Greene, R. W., et al. (2016) · Nature · doi:10.1038/nature19325 · Cited by 827
Intact-brain analyses reveal distinct information carried by SNc dopamine subcircuits
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., et al. (2015) · Cell · doi:10.1016/j.cell.2015.07.014 · Cited by 794
“…CLARITY-optimized light-sheet microscopy (COLM) (Chung et al., 2013; Tomer et al., 2014), along with a variation of rabies-based circuit mapping (Schwarz et al., 2015); the lattermethod (TRIO) operates similarly to previously published rabies-based circuit mapping technologies, utilizing a…”
MethodSelf-citationZingg, B., Chou, X.-L., Zhang, Z., Mesik, L., Liang, F., Tao, H. W., & Zhang, L. I. (2016) · Neuron · doi:10.1016/j.neuron.2016.11.045 · Cited by 775
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Poe, G. R., Foote, S., Eschenko, O., Johansen, J. P., Bouret, S., Aston-Jones, G., Harley, C. W., Manahan-Vaughan, D., Weinshenker, D., Valentino, R., et al. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-0360-9 · Cited by 720
Integration of optogenetics with complementary methodologies in systems neuroscience
Kim, C. K., Adhikari, A., & Deisseroth, K. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2017.15 · Cited by 690
Organization of the Locus Coeruleus-Norepinephrine System
Schwarz, L. A., & Luo, L. (2015) · Current Biology · doi:10.1016/j.cub.2015.09.039 · Cited by 578
Self-citationA genetically encoded fluorescent sensor for rapid and specific in vivo detection of norepinephrine
Feng, J., Zhang, C., Lischinsky, J. E., Jing, M., Zhou, J., Wang, H., Zhang, Y., Dong, A., Wu, Z., Wu, H., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.02.037 · Cited by 545
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Daviu, N., Bruchas, M. R., Moghaddam, B., Sandi, C., & Beyeler, A. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2019.100191 · Cited by 591
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Fernandez, D. C., Fogerson, P. M., Lazzerini Ospri, L., Thomsen, M. B., Layne, R. M., Severin, D., Zhan, J., Singer, J. H., Kirkwood, A., Zhao, H., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.004 · Cited by 505
Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems
Ren, J., Friedmann, D., Xiong, J., Liu, C. D., Ferguson, B. R., Weerakkody, T., DeLoach, K. E., Ran, C., Pun, A., Sun, Y., et al. (2018) · Cell · doi:10.1016/j.cell.2018.07.043 · Cited by 498
Self-citationCerebellar granule cells encode the expectation of reward
Wagner, M. J., Kim, T. H., Savall, J., Schnitzer, M. J., & Luo, L. (2017) · Nature · doi:10.1038/nature21726 · Cited by 505
Self-citationFunctional circuit architecture underlying parental behaviour
Kohl, J., Babayan, B. M., Rubinstein, N. D., Autry, A. E., Marin-Rodriguez, B., Kapoor, V., Miyamichi, K., Zweifel, L. S., Luo, L., Uchida, N., et al. (2018) · Nature · doi:10.1038/s41586-018-0027-0 · Cited by 470
Self-citationGenetic Dissection of Neural Circuits: A Decade of Progress
Luo, L., Callaway, E. M., & Svoboda, K. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.040 · Cited by 454
Self-citationMonosynaptic Circuit Tracing with Glycoprotein-Deleted Rabies Viruses
Callaway, E. M., & Luo, L. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0409-15.2015 · Cited by 418
Self-citationEliava, M., Melchior, M., Knobloch-Bollmann, H. S., Wahis, J., da Silva Gouveia, M., Tang, Y., Ciobanu, A. C., Triana del Rio, R., Roth, L. C., Althammer, F., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.041 · Cited by 409
Architectures of neuronal circuits
Luo, L. (2021) · Science · doi:10.1126/science.abg7285 · Cited by 390
Self-citationNeuromodulation by the immune system: a focus on cytokines
Salvador, A. F., de Lima, K. A., & Kipnis, J. (2021) · Nature Reviews Immunology · doi:10.1038/s41577-021-00508-z · Cited by 389
High-throughput mapping of single-neuron projections by sequencing of barcoded RNA
Kebschull, J. M., Garcia da Silva, P., Reid, A. P., Peikon, I. D., Albeanu, D. F., & Zador, A. M. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.036 · Cited by 376
Farmer, A. D., Strzelczyk, A., Finisguerra, A., Gourine, A. V., Gharabaghi, A., Hasan, A., Burger, A. M., Jaramillo, A. M., Mertens, A., Majid, A., et al. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2020.568051 · Cited by 375
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François, A., Low, S. A., Sypek, E. I., Christensen, A. J., Sotoudeh, C., Beier, K. T., Ramakrishnan, C., Ritola, K., Sharif‐Naeini, R., Deisseroth, K. A., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.01.008 · Cited by 368
Self-citationActive control of arousal by a locus coeruleus GABAergic circuit
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Uematsu, A., Tan, B. Z., Ycu, E. A., Cuevas, J. N. S., Koivumaa, J., Junyent, F., Kremer, E. J., Witten, I. B., Deisseroth, K. A., & Johansen, J. P. (2017) · Nature Neuroscience · doi:10.1038/nn.4642 · Cited by 356
Self-citationLocus coeruleus to basolateral amygdala noradrenergic projections promote anxiety-like behavior
McCall, J. G., Siuda, E. R., Bhatti, D. L., Lawson, L. A., McElligott, Z. A., Stuber, G. D., & Bruchas, M. R. (2017) · eLife · doi:10.7554/elife.18247 · Cited by 342
Rapid Reconfiguration of the Functional Connectome after Chemogenetic Locus Coeruleus Activation
Zerbi, V., Floriou‐Servou, A., Markicevic, M., Vermeiren, Y., Sturman, O., Privitera, M., von Ziegler, L., Ferrari, K. D., Weber, B., Deyn, P. P. D., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.034 · Cited by 343
Susaki, E. A., & Ueda, H. R. (2016) · Cell chemical biology · doi:10.1016/j.chembiol.2015.11.009 · Cited by 304
Breathing control center neurons that promote arousal in mice
Yackle, K., Schwarz, L. A., Kam, K., Sorokin, J. M., Huguenard, J. R., Feldman, J. L., Luo, L., & Krasnow, M. A. (2017) · Science · doi:10.1126/science.aai7984 · Cited by 282
Self-citationDistinct Ventral Pallidal Neural Populations Mediate Separate Symptoms of Depression
Knowland, D., Lilascharoen, V., Pacia, C. P., Shin, S., Wang, E. H.-J., & Lim, B. K. (2017) · Cell · doi:10.1016/j.cell.2017.06.015 · Cited by 273
Locus coeruleus: From global projection system to adaptive regulation of behavior
Aston‐Jones, G., & Waterhouse, B. D. (2016) · Brain Research · doi:10.1016/j.brainres.2016.03.001 · Cited by 268
Cellular anatomy of the mouse primary motor cortex
Muñoz-Castañeda, R., Zingg, B., Matho, K. S., Chen, X., Wang, Q., Foster, N. N., Li, A., Narasimhan, A., Hirokawa, K. E., Huo, B., et al. (2021) · Nature · doi:10.1038/s41586-021-03970-w · Cited by 265
Central amygdala circuits modulate food consumption through a positive-valence mechanism
Douglass, A. M., Kucukdereli, H., Ponserre, M., Marković, M., Gründemann, J., Strobel, C., Morales, P. L. A., Conzelmann, K., Lüthi, A., & Klein, R. (2017) · Nature Neuroscience · doi:10.1038/nn.4623 · Cited by 264
Dendritic spines: Revisiting the physiological role
Chidambaram, S. B., Rathipriya, A. G., Bolla, S. R., Bhat, A., Ray, B., Mahalakshmi, A. M., Manivasagam, T., Thenmozhi, A. J., Essa, M. M., Guillemin, G. J., et al. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.01.005 · Cited by 266
Locus coeruleus norepinephrine activity mediates sensory-evoked awakenings from sleep
Hayat, H., Regev, N., Matosevich, N., Sales, A. C., Paredes-Rodriguez, E., Krom, A. J., Bergman, L., Li, Y., Lavigne, M., Kremer, E. J., et al. (2020) · Science Advances · doi:10.1126/sciadv.aaz4232 · Cited by 268
Self-citationHu, H. (2016) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-014106 · Cited by 253
Cerebellar nuclei evolved by repeatedly duplicating a conserved cell-type set
Kebschull, J. M., Richman, E. B., Ringach, N., Friedmann, D., Albarran, E., Kolluru, S. S., Jones, R. C., Allen, W. E., Wang, Y., Cho, S. W., et al. (2020) · Science · doi:10.1126/science.abd5059 · Cited by 262
Self-citationHirschberg, S., Li, Y., Randall, A. D., Kremer, E. J., & Pickering, A. E. (2017) · eLife · doi:10.7554/elife.29808 · Cited by 252
Self-citationFujita, H., Kodama, T., & du Lac, S. (2020) · eLife · doi:10.7554/elife.58613 · Cited by 254
The emergence and influence of internal states
Flavell, S. W., Gogolla, N., Lovett-Barron, M., & Zelikowsky, M. (2022) · Neuron · doi:10.1016/j.neuron.2022.04.030 · Cited by 246
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Gielow, M. R., & Záborszky, L. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.01.060 · Cited by 243
Rorabaugh, J. M., Chalermpalanupap, T., Botz-Zapp, C. A., Fu, V. M., Lembeck, N. A., Cohen, R. M., & Weinshenker, D. (2017) · Brain · doi:10.1093/brain/awx232 · Cited by 227
Chandler, D. J., Jensen, P., McCall, J. G., Pickering, A. E., Schwarz, L. A., & Totah, N. K. B. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1164-19.2019 · Cited by 229
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Zhou, Z., Liu, X., Chen, S., Zhang, Z., Liu, Y., Montardy, Q., Tang, Y., Wei, P., Liu, N., Li, L., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.027 · Cited by 221
The diversity of GABAergic neurons and neural communication elements
Huang, Z. J., & Paul, A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0195-4 · Cited by 201
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Lipton, D. M., Gonzales, B. J., & Citri, A. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00028 · Cited by 222
Noradrenergic Modulation of Fear Conditioning and Extinction
Giustino, T. F., & Maren, S. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00043 · Cited by 203
Synaptic Specificity and Application of Anterograde Transsynaptic AAV for Probing Neural Circuitry
Zingg, B., Peng, B., Huang, J., Tao, H. W., & Zhang, L. I. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2158-19.2020 · Cited by 197
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Surmeier, D. J., Obeso, J. A., & Halliday, G. M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1787-16.2017 · Cited by 197
A labeled-line neural circuit for pheromone-mediated sexual behaviors in mice
Ishii, K. K., Osakada, T., Mori, H., Miyasaka, N., Yoshihara, Y., Miyamichi, K., & Touhara, K. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.038 · Cited by 185
Self-citationThe Locus Coeruleus Is a Complex and Differentiated Neuromodulatory System
Totah, N. K., Neves, R. M., Panzeri, S., Logothetis, N. K., & Eschenko, O. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.037 · Cited by 179
Shared cortex-cerebellum dynamics in the execution and learning of a motor task
Wagner, M. J., Kim, T. H., Kadmon, J., Nguyen, N. D., Ganguli, S., Schnitzer, M. J., & Luo, L. (2019) · Cell · doi:10.1016/j.cell.2019.02.019 · Cited by 177
Self-citationSun, Q., Li, X., Ren, M., Zhao, M., Zhong, Q., Ren, Y., Luo, P., Ni, H., Zhang, X., Zhang, C., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0429-9 · Cited by 180
The Role of the Locus Coeruleus in Pain and Associated Stress-Related Disorders
Suárez‐Pereira, I., Llorca-Torralba, M., Bravo, L., Camarena-Delgado, C., Soriano‐Mas, C., & Berrocoso, E. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.11.023 · Cited by 181
Nontoxic, double-deletion-mutant rabies viral vectors for retrograde targeting of projection neurons
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., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0091-7 · Cited by 177
Breton‐Provencher, V., Drummond, G. T., & Sur, M. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.638007 · Cited by 182
Viral Strategies for Targeting the Central and Peripheral Nervous Systems
Bedbrook, C. N., Deverman, B. E., & Gradinaru, V. (2018) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-080317-062048 · Cited by 168
Osorio-Forero, A., Foustoukos, G., Cardis, R., Cherrad, N., Devenoges, C., Fernandez, L. M. J., & Lüthi, A. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01822-0 · Cited by 175
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Staiger, J. F., & Petersen, C. C. H. (2021) · Physiological Reviews · doi:10.1152/physrev.00019.2019 · Cited by 165
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Likhtik, E., & Johansen, J. P. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0503-3 · Cited by 169
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Paredes-Rodriguez, E., Vegas‐Suárez, S., Morera‐Herreras, T., Deurwaerdère, P. D., & Miguélez, C. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.00435 · Cited by 165
Consensus Paper: Experimental Neurostimulation of the Cerebellum
Miterko, L. N., Baker, K. B., Beckinghausen, J., Bradnam, L. V., Cheng, M., Cooperrider, J., DeLong, M. R., Gornati, S. V., Hallett, M., Heck, D. H., et al. (2019) · The Cerebellum · doi:10.1007/s12311-019-01041-5 · Cited by 165
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Atlan, G., Terem, A., Peretz‐Rivlin, N., Sehrawat, K., Gonzales, B. J., Pozner, G., Tasaka, G., Goll, Y., Refaeli, R., Zviran, O., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.06.068 · Cited by 160
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Lerner, T. N., Ye, L., & Deisseroth, K. (2016) · Cell · doi:10.1016/j.cell.2016.02.027 · Cited by 159
Nectow, A. R., & Nestler, E. J. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-00382-z · Cited by 159
Circuit and molecular architecture of a ventral hippocampal network
Gergues, M. M., Han, K. J., Choi, H. S., Brown, B., Clausing, K. J., Turner, V. S., Vainchtein, I. D., Molofsky, A. V., & Kheirbek, M. A. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0705-8 · Cited by 158
Organization of the inputs and outputs of the mouse superior colliculus
Benavidez, N. L., Bienkowski, M. S., Zhu, M., Garcia, L., Fayzullina, M., Gao, L., Bowman, I., Gou, L., Khanjani, N., Cotter, K. R., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24241-2 · Cited by 159
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Dahl, M. J., Mather, M., & Werkle‐Bergner, M. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2021.10.009 · Cited by 165
Rompani, S. B., Müllner, F. E., Wanner, A. A., Zhang, C., Roth, C. N., Yonehara, K., & Roska, B. (2017) · Neuron · doi:10.1016/j.neuron.2017.01.028 · Cited by 156
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Krohn, F., Novello, M., van der Giessen, R. S., Zeeuw, C. I. D., Pel, J. J. M., & Bosman, L. W. J. (2023) · eLife · doi:10.7554/elife.83654 · Cited by 164
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Saleeba, C., Dempsey, B., Le, S., Goodchild, A., & McMullan, S. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00897 · Cited by 153
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Salkoff, D. B., Zagha, E., McCarthy, E., & McCormick, D. A. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz206 · Cited by 157
Kim, J., Jung, A.-H., Jeong, D., Choi, I., Kim, K., Shin, S., Kim, S. J., & Lee, S. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4333-15.2016 · Cited by 148
Vagus nerve stimulation induces widespread cortical and behavioral activation
Collins, L. N., Boddington, L. J., Steffan, P. J., & McCormick, D. A. (2021) · Current Biology · doi:10.1016/j.cub.2021.02.049 · Cited by 153
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Tetzlaff, S. K., Reyhan, E., Layer, N., Bengtson, C. P., Heuer, A., Schroers, J., Faymonville, A. J., Langeroudi, A. P., Drewa, N., Keifert, E., et al. (2024) · Cell · doi:10.1016/j.cell.2024.11.002 · Cited by 155
Qi, G., Zhang, P., Li, T., Li, M., Zhang, Q., He, F., Zhang, L., Cai, H., Lv, X., Qiao, H., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28190-2 · Cited by 151
Functions and dysfunctions of neocortical inhibitory neuron subtypes
Hattori, R., Kuchibhotla, K. V., Froemke, R. C., & Komiyama, T. (2017) · Nature Neuroscience · doi:10.1038/nn.4619 · Cited by 149
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Soya, S., Takahashi, T. M., McHugh, T. J., Maejima, T., Herlitze, S., Abe, M., Sakimura, K., & Sakurai, T. (2017) · Nature Communications · doi:10.1038/s41467-017-01782-z · Cited by 149
Cholinergic modulation of spatial learning, memory and navigation
Solari, N., & Hangya, B. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14089 · Cited by 146
Connectional architecture of a mouse hypothalamic circuit node controlling social behavior
Lo, L., Yao, S., Kim, D., Cetin, A. H., Harris, J. A., Zeng, H., Anderson, D. J., & Weissbourd, B. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1817503116 · Cited by 141
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Chen, K.-S., Xu, M., Zhang, Z., Chang, W.-C., Gaj, T., Schaffer, D. V., & Dan, Y. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.005 · Cited by 145
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Raam, T., & Hong, W. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.02.008 · Cited by 134
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Clopath, C., Bonhoeffer, T., Hübener, M., & Rose, T. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0161 · Cited by 137
Egroo, M. V., Koshmanova, E., Vandewalle, G., & Jacobs, H. I. L. (2022) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2022.101592 · Cited by 146
Genetically identified amygdala–striatal circuits for valence-specific behaviors
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Jordan, R., & Keller, G. B. (2023) · eLife · doi:10.7554/elife.85111 · Cited by 127
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Blot, A., Roth, M., Gasler, I. T., Javadzadeh, M., Imhof, F., & Hofer, S. B. (2021) · Neuron · doi:10.1016/j.neuron.2021.04.017 · Cited by 129
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Feng, J., Dong, H., Lischinsky, J. E., Zhou, J., Deng, F., Zhuang, C., Miao, X., Wang, H., Li, G., Cai, R., et al. (2024) · Neuron · doi:10.1016/j.neuron.2024.03.001 · Cited by 122
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Xu, X., Holmes, T. C., Luo, M., Beier, K. T., Horwitz, G. D., Zhao, F., Zeng, W., Hui, M., Semler, B. L., & Sandri-Goldin, R. M. (2020) · Neuron · doi:10.1016/j.neuron.2020.07.010 · Cited by 126
Self-citationDifferential Encoding in Prefrontal Cortex Projection Neuron Classes Across Cognitive Tasks
Lui, J. H., Nguyen, N. D., Grutzner, S. M., Darmanis, S., Peixoto, D., Wagner, M. J., Allen, W. E., Kebschull, J. M., Richman, E. B., Ren, J., et al. (2020) · Cell · doi:10.1016/j.cell.2020.11.046 · Cited by 124
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Mo, C., & Sherman, S. M. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1467-18.2018 · Cited by 118
Beier, K. T., Gao, X. J., Xie, S. C., DeLoach, K. E., Malenka, R. C., & Luo, L. (2019) · Cell Reports · doi:10.1016/j.celrep.2018.12.040 · Cited by 126
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Metadata
- Authors
- Schwarz, L. A., Miyamichi, K., Gao, X. J., Beier, K. T., Weissbourd, B., DeLoach, K. E., Ren, J., Ibanes, S., Malenka, R. C., Kremer, E. J., & Luo, L.
- Affiliations
- Howard Hughes Medical Institute (US)
- Centre National de la Recherche Scientifique (FR)
- Stanford Medicine (US)
- Corresponding author
- Luo, Liqun
- ORCID
- Venue
- Nature
- Published
- 2015-07-01
- Volume
- 524
- Issue
- 7563
- Pages
- 88-92
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4587569
- OpenAlex
- W2099401565
- Cited by
- 744
- References
- 40
- Citations by year
- 2026: 48 · 2025: 74 · 2024: 64 · 2023: 85 · 2022: 67 · 2021: 77 · 2020: 85 · 2019: 78 · 2018: 55 · 2017: 55 · 2016: 38 · 2015: 16
- FWCI
- 25.50
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Science Foundation
- Howard Hughes Medical Institute
- Agence Nationale de la Recherche (ANR-10-LABX-0012)
- Stanford Bio-X
- National Institute of Mental Health
- National Institute on Drug Abuse (F32DA038913, P01DA008227)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- locus coeruleus, noradrenergic neurons, norepinephrine, rabies virus tracing, transsynaptic tracing, Purkinje cells, neuronal projection patterns, mice, brain states, spinal cord projections, sensory gating
- MeSH terms
- Animals, Axons, Brain, Female, Locus Coeruleus, Male, Neural Pathways, Neurons, Norepinephrine, Pilot Projects, Purkinje Cells, Rabies virus, Synapses, Reproducibility of Results, Rats, Wistar, Mice, Rats, Neuroanatomical Tract-Tracing Techniques
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