Systematic comparison of adeno‐associated virus and biotinylated dextran amine reveals equivalent sensitivity between tracers and novel projection targets in the mouse brain
Abstract
As an anterograde neuronal tracer, recombinant adeno‐associated virus (AAV) has distinct advantages over the widely used biotinylated dextran amine (BDA). However, the sensitivity and selectivity of AAV remain uncharacterized for many brain regions and species. To validate this tracing method further, AAV (serotype 1) was systematically compared with BDA as an anterograde tracer by injecting both tracers into three cortical and 15 subcortical regions in C57BL/6J mice. Identical parameters were used for our sequential iontophoretic injections, producing injections of AAV that were more robust in size and in density of neurons infected compared with those of BDA. However, these differences did not preclude further comparison between the tracers, because the pairs of injections were suitably colocalized and contained some percentage of double‐labeled neurons. A qualitative analysis of projection patterns showed that the two tracers behave very similarly when injection sites are well matched. Additionally, a quantitative analysis of relative projection intensity for cases targeting primary motor cortex (MOp), primary somatosensory cortex (SSp), and caudoputamen (CP) showed strong agreement in the ranked order of projection intensities between the two tracers. A detailed analysis of the projections of two brain regions (SSp and MOp) revealed many targets that have not previously been described in the mouse or rat. Minor retrograde labeling of neurons was observed in all cases examined, for both AAV and BDA. Our results show that AAV has actions equivalent to those of BDA as an anterograde tracer and is suitable for analysis of neural circuitry throughout the mouse brain. J. Comp. Neurol. 522:1989–2012, 2014. © 2014 Wiley Periodicals, Inc.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
AAV was at least as efficient as, and more specific than, the classic anterograde tracer BDA.
“We also confirmed that AAV was at least as efficient as, and more specific than, the classic anterograde tracer biotinylated dextran amine (BDA) (Extended Data Fig. 1), as described separately21.”
From A mesoscale connectome of the mouse brain (2014) · cites this paper as [21]
Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
Distributed hierarchical processing in the primate cerebral cortex
Felleman, D. J., & Van Essen, D. C. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1 · Cited by 7,783 · see citing works
Genome-wide atlas of gene expression in the adult mouse brain
Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., et al. (2007) · Nature · doi:10.1038/nature05453 · Cited by 5,572 · see citing works
Self-citationThe Human Connectome: A Structural Description of the Human Brain
Sporns, O., Tononi, G., & Kötter, R. (2005) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0010042 · Cited by 3,260 · see citing works
An anatomically comprehensive atlas of the adult human brain transcriptome
Hawrylycz, M. J., Lein, E. S., Guillozet-Bongaarts, A. L., Shen, E. H., Ng, L., Miller, J. A., van de Lagemaat, L. N., Smith, K. A., Ebbert, A., Riley, Z. L., et al. (2012) · Nature · doi:10.1038/nature11405 · Cited by 3,083 · see citing works
Self-citationA mesoscale connectome of the mouse brain
Oh, S. W., Harris, J. A., Ng, L., Winslow, B., Cain, N., Mihalas, S., Wang, Q., Lau, C., Kuan, L., Henry, A. M., et al. (2014) · Nature · doi:10.1038/nature13186 · Cited by 2,612 · see citing works
Self-citationFink, R., & Heimer, L. (1967) · Brain Research · doi:10.1016/0006-8993(67)90166-7 · Cited by 1,766 · see citing works
Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat
Hoover, W. B., & Vertes, R. P. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0150-4 · Cited by 1,365 · see citing works
A new neural framework for visuospatial processing
Kravitz, D. J., Saleem, K. S., Baker, C. I., & Mishkin, M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3008 · Cited by 1,325 · see citing works
Gerfen, C. R., & Sawchenko, P. E. (1984) · Brain Research · doi:10.1016/0006-8993(84)90940-5 · Cited by 1,203 · see citing works
The ventral visual pathway: an expanded neural framework for the processing of object quality
Kravitz, D. J., Saleem, K. S., Baker, C. I., Ungerleider, L. G., & Mishkin, M. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.10.011 · Cited by 1,154 · see citing works
Adeno-associated Virus Serotypes: Vector Toolkit for Human Gene Therapy
Wu, Z., Asokan, A., & Samulski, R. J. (2006) · Molecular Therapy · doi:10.1016/j.ymthe.2006.05.009 · Cited by 921 · see citing works
Genetic Dissection of Neural Circuits
Luo, L., Callaway, E. M., & Svoboda, K. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.002 · Cited by 754 · see citing works
Burger, C., Gorbatyuk, O. S., Velardo, M. J., Peden, C. S., Williams, P., Zolotukhin, S., Reier, P. J., Mandel, R. J., & Muzyczka, N. (2004) · Molecular Therapy · doi:10.1016/j.ymthe.2004.05.024 · Cited by 741 · see citing works
Serial two-photon tomography for automated ex vivo mouse brain imaging
Ragan, T. M., Kadiri, L. R., Venkataraju, K. U., Bahlmann, K., Sutin, J. D. B., Taranda, J., Arganda‐Carreras, I., Kim, Y., Seung, H. S., & Osten, P. (2012) · Nature Methods · doi:10.1038/nmeth.1854 · Cited by 659 · see citing works
Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin
Kawaguchi, Y., Wilson, C. J., & Emson, P. C. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-10-03421.1990 · Cited by 569 · see citing works
Gerfen, C. R. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902360404 · Cited by 563 · see citing works
Aschauer, D. F., Kreuz, S., & Rumpel, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076310 · Cited by 522 · see citing works
Retrograde axonal transport of protein
Kristensson, K., & Olsson, Y. (1971) · Brain Research · doi:10.1016/0006-8993(71)90044-8 · Cited by 519 · see citing works
Long-Range Neuronal Circuits Underlying the Interaction between Sensory and Motor Cortex
Mao, T., Kusefoglu, D., Hooks, B. M., Huber, D., Petreanu, L., & Svoboda, K. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.029 · Cited by 514 · see citing works
Lateral Connectivity and Contextual Interactions in Macaque Primary Visual Cortex
Stettler, D. D., Das, A., Bennett, J., & Gilbert, C. D. (2002) · Neuron · doi:10.1016/s0896-6273(02)01029-2 · Cited by 506 · see citing works
Area map of mouse visual cortex
Wang, Q., & Burkhalter, A. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21286 · Cited by 498 · see citing works
Self-citationFunctional Specialization of Seven Mouse Visual Cortical Areas
Marshel, J. H., Garrett, M., Nauhaus, I., & Callaway, E. M. (2011) · Neuron · doi:10.1016/j.neuron.2011.12.004 · Cited by 467 · see citing works
Zeng, H., Shen, E. H., Hohmann, J. G., Oh, S. W., Bernard, A., Royall, J. J., Glattfelder, K. J., Sunkin, S. M., Morris, J. A., Guillozet-Bongaarts, A. L., et al. (2012) · Cell · doi:10.1016/j.cell.2012.02.052 · Cited by 426 · see citing works
Self-citationCurrent concepts in neuroanatomical tracing
Köbbert, C., Apps, R., Bechmann, I., Lanciego, J. L., Mey, J., & Thanos, S. (2000) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00019-8 · Cited by 419 · see citing works
Wang, Q., Sporns, O., & Burkhalter, A. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.6063-11.2012 · Cited by 410 · see citing works
Self-citationFunctional specialization of mouse higher visual cortical areas
Andermann, M. L., Kerlin, A. M., Roumis, D. K., Glickfeld, L. L., & Reid, R. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.11.013 · Cited by 406 · see citing works
Bourassa, J., Pinault, D., & Deschênes, M. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb01016.x · Cited by 405 · see citing works
Tennant, K. A., Adkins, D. L., Donlan, N. A., Asay, A. L., Thomas, N. J., Kleim, J. A., & Jones, T. A. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq159 · Cited by 403 · see citing works
Textura del Sistema Nervioso del Hombre y de los Vertebrados, 1899–1904
y Cajal, S. R. (2019) · Princeton University Press eBooks · doi:10.1515/9780691183978-016 · Cited by 382 · see citing works
Michaela, E., & Elphick, M. R. (2000) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(20000626)422:2 · Cited by 364 · see citing works
Hattox, A. M., & Nelson, S. B. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00397.2007 · Cited by 344 · see citing works
Organization of Cortical and Thalamic Input to Pyramidal Neurons in Mouse Motor Cortex
Hooks, B. M., Mao, T., Gutnisky, D. A., Yamawaki, N., Svoboda, K., & Shepherd, G. M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4338-12.2013 · Cited by 343 · see citing works
Pathway tracing using biotinylated dextran amines
Reiner, A. J., Veenman, C. L., Medina, L. M., Jiao, Y., Mar, N. D., & Honig, M. G. (2000) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(00)00293-4 · Cited by 343 · see citing works
Long‐range connectivity of mouse primary somatosensory barrel cortex
Aronoff, R., Matyas, F., Mateo, C., Ciron, C., Schneider, B., & Petersen, C. C. H. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07264.x · Cited by 323 · see citing works
Terminal Degeneration within the Central Nervous System as Studied by a New Silver Method
Glees, P. (1946) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-194601000-00005 · Cited by 311 · see citing works
Canteras, N. S., Shammah‐Lagnado, S. J., Silva, B. A., & Ricardo, J. A. (1990) · Brain Research · doi:10.1016/0006-8993(90)91087-w · Cited by 306 · see citing works
Comparative Analysis of Adeno-Associated Viral Vector Serotypes 1, 2, 5, 7, And 8 in Mouse Brain
Taymans, J.-M., Vandenberghe, L. H., Haute, C. V. D., Thiry, I., Deroose, C. M., Mortelmans, L., Wilson, J. M., Debyser, Z., & Baekelandt, V. (2007) · Human Gene Therapy · doi:10.1089/hum.2006.178 · Cited by 305 · see citing works
Nathanson, J. L., Yanagawa, Y., Obata, K., & Callaway, E. M. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.03.032 · Cited by 305 · see citing works
MR connectomics: Principles and challenges
Hagmann, P., Cammoun, L., Gigandet, X., Gerhard, S., Grant, P. E., Wedeen, V. J., Meuli, R. A., Thiran, J., Honey, C. J., & Sporns, O. (2010) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2010.01.014 · Cited by 271 · see citing works
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., et al. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000334 · Cited by 261 · see citing works
Self-citationHierarchical organization of areas in rat visual cortex
Coogan, T. A., & Burkhalter, A. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03749.1993 · Cited by 260 · see citing works
Axons and synaptic boutons are highly dynamic in adult visual cortex
Stettler, D. D., Yamahachi, H., Li, W., Denk, W., & Gilbert, C. D. (2006) · Neuron · doi:10.1016/j.neuron.2006.02.018 · Cited by 256 · see citing works
Mapping brain circuitry with a light microscope
Osten, P., & Margrie, T. W. (2013) · Nature Methods · doi:10.1038/nmeth.2477 · Cited by 244 · see citing works
Nauta, W. J. H., & Gygax, P. A. (1951) · Stain Technology · doi:10.3109/10520295109113170 · Cited by 244 · see citing works
Application of Silver Degeneration Stains for Neurotoxicity Testing
Switzer, R. C. (2000) · Toxicologic Pathology · doi:10.1177/019262330002800109 · Cited by 242 · see citing works
Gateways of Ventral and Dorsal Streams in Mouse Visual Cortex
Wang, Q., Gao, E., & Burkhalter, A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3488-10.2011 · Cited by 232 · see citing works
Self-citationBiotin-dextran: a sensitive anterograde tracer for neuroanatomic studies in rat and monkey
Brandt, H., & Apkarian, A. V. (1992) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(92)90041-b · Cited by 226 · see citing works
White, E. L., & DeAmicis, R. A. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901750405 · Cited by 222 · see citing works
Chamberlin, N. L., Du, B., de Lacalle, S., & Saper, C. B. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00169-3 · Cited by 221 · see citing works
A half century of experimental neuroanatomical tracing
Lanciego, J. L., & Wouterlood, F. G. (2011) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2011.07.001 · Cited by 215 · see citing works
Laminar Analysis of Excitatory Local Circuits in Vibrissal Motor and Sensory Cortical Areas
Hooks, B. M., Hires, S. A., Zhang, Y.-X., Huber, D., Petreanu, L., Svoboda, K., & Shepherd, G. M. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000572 · Cited by 214 · see citing works
Wu, Y., Richard, S., & Parent, A. (2000) · Neuroscience Research · doi:10.1016/s0168-0102(00)00140-1 · Cited by 213 · see citing works
Genetic Approaches to Neural Circuits in the Mouse
Josh Huang, Z., & Zeng, H. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170307 · Cited by 200 · see citing works
Self-citationBakowska, J. C., & Morrell, J. I. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970922)386:2 · Cited by 198 · see citing works
The future of the human connectome
Essen, D. C. V., & Uǧurbil, K. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.01.032 · Cited by 192 · see citing works
Fluorescent dextran-amines used as axonal tracers in the nervous system of the chicken embryo
Glover, J. C., Pétursdóttir, G., & Jansen, J. K. S. (1986) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(86)90011-7 · Cited by 191 · see citing works
Expanded Repertoire of AAV Vector Serotypes Mediate Unique Patterns of Transduction in Mouse Brain
Cearley, C. N., Vandenberghe, L. H., Parente, M. K., Carnish, E. R., Wilson, J. M., & Wolfe, J. H. (2008) · Molecular Therapy · doi:10.1038/mt.2008.166 · Cited by 182 · see citing works
Hoogland, P. V. J. M., Welker, E., & der Loos, H. V. (1987) · Experimental Brain Research · doi:10.1007/bf00255235 · Cited by 178 · see citing works
Wouterlood, F. G., & Jorritsma‐Byham, B. (1993) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(05)80009-3 · Cited by 178 · see citing works
Nauta, W. J. H., & Gygax, P. A. (1993) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4684-7920-1_1 · Cited by 178 · see citing works
Input-output organization of the rat vibrissal motor cortex
Miyashita, E., Keller, A., & Asanuma, H. (1994) · Experimental Brain Research · doi:10.1007/bf00239589 · Cited by 174 · see citing works
Functional circuitry involved in the regulation of whisker movements
Hattox, A. M., Priest, C. A., & Keller, A. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.10089 · Cited by 167 · see citing works
Biotinylated dextran: a versatile anterograde and retrograde neuronal tracer
Rajakumar, N., Elisevich, K. V., & Flumerfelt, B. A. (1993) · Brain Research · doi:10.1016/0006-8993(93)91488-e · Cited by 166 · see citing works
Thompson, R. H., & Swanson, L. W. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009112107 · Cited by 158 · see citing works
Smith, Y., & Parent, A. (1986) · Brain Research · doi:10.1016/0006-8993(86)91131-5 · Cited by 146 · see citing works
Hoogland, P. V. J. M., Wouterlood, F. G., Welker, E., & der Loos, H. V. (1991) · Experimental Brain Research · doi:10.1007/bf00228517 · Cited by 143 · see citing works
Afferent and efferent pathways of the vibrissal region of primary motor cortex in the mouse
Porter, L. L., & White, E. L. (1983) · Journal of Comparative Neurology · doi:10.1002/cne.902140306 · Cited by 131 · see citing works
Welker, E., Hoogland, P., & van der Loos, H. (2004) · Experimental Brain Research · doi:10.1007/bf00248234 · Cited by 117 · see citing works
Adeno-Associated Viral Vectors for Mapping, Monitoring, and Manipulating Neural Circuits
Betley, J. N., & Sternson, S. M. (2011) · Human Gene Therapy · doi:10.1089/hum.2010.204 · Cited by 102 · see citing works
Thalamic connectivity of rat somatic motor cortex
Aldes, L. D. (1988) · Brain Research Bulletin · doi:10.1016/0361-9230(88)90063-9 · Cited by 95 · see citing works
Wright, A. K., Norrie, L., Ingham, C. A., Hutton, E. A. M., & Arbuthnott, G. W. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00186-9 · Cited by 93 · see citing works
Chen, S., & Aston‐Jones, G. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00336-9 · Cited by 85 · see citing works
Gautron, L., Lazarus, M., Scott, M. M., Saper, C. B., & Elmquist, J. K. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22323 · Cited by 82 · see citing works
Alloway, K. D., Li, L., Nwabueze-Ogbo, F. C., & Chakrabarti, S. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21039 · Cited by 78 · see citing works
Macrophage and microglia-like cells in the avian inner ear
Bhave, S. A., Oesterle, E. C., & Coltrera, M. D. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980824)398:2 · Cited by 77 · see citing works
Tanigawa, H., Wang, Q., & Fujita, I. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi067 · Cited by 74 · see citing works
Self-citationHarris, J. A., Wook Oh, S., & Zeng, H. (2012) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0120s59 · Cited by 72 · see citing works
Self-citationHigh-resolution gene expression atlases for adult and developing mouse brain and spinal cord
Henry, A. M., & Hohmann, J. G. (2012) · Mammalian Genome · doi:10.1007/s00335-012-9406-2 · Cited by 70 · see citing works
Self-citationRat whisker motor cortex is subdivided into sensory-input and motor-output areas
Smith, J., & Alloway, K. (2013) · Front. Neural Circuits · doi:10.3389/fncir.2013.00004 · Cited by 65 · see citing works
Hoover, J. E., Hoffer, Z. S., & Alloway, K. D. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01009.2002 · Cited by 61 · see citing works
Almeida, A., COBOS, A. R., Tavares, I., & Lima, D. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02058.x · Cited by 59 · see citing works
Quantitative Aspects of Corticocortical Connections: A Tracer Study in the Mouse
Schüz, A., Chaimow, D., Liewald, D., & Dortenmann, M. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhj085 · Cited by 52 · see citing works
Thompson, S. M., Fortunato, C., McKinney, R. A., M�ller, M., & G�hwiler, B. H. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960902)372:4 · Cited by 45 · see citing works
Shin, S., & Sommer, M. A. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00101.2009 · Cited by 43 · see citing works
Cadusseau, J., & Roger, M. (1991) · Neuroscience Research · doi:10.1016/0168-0102(91)90102-5 · Cited by 38 · see citing works
Larsen, D. D. (2009) · Frontiers in Neuroanatomy · doi:10.3389/neuro.05.030.2009 · Cited by 38 · see citing works
Alloway, K. D., Smith, J. B., & Beauchemin, K. J. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22477 · Cited by 37 · see citing works
Haque, T., Yamamoto, S., Masuda, Y., Kato, T., Sato, F., Uchino, K., Oka, A., Nakamura, M., Takeda, R., Ono, T., et al. (2010) · Brain Research · doi:10.1016/j.brainres.2010.05.034 · Cited by 30 · see citing works
Anterograde Axonal Tract Tracing
Raju, D. V., & Smith, Y. (2006) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0114s37 · Cited by 29 · see citing works
Paulussen, M., Jacobs, S., der Gucht, E. V., Hof, P. R., & Arckens, L. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0311-3 · Cited by 26 · see citing works
Ling, C., Hendrickson, M. L., & Kalil, R. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045886 · Cited by 12 · see citing works
Direct striatothalamic projections in the neonatal rat
Hattori, T., Takada, M., Moriizumi, T., & Campbell, K. J. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90074-9 · Cited by 6 · see citing works
Hagihara (1999) · doi:10.1002/(sici)1096-9861(19990726)410:2
Flagged first, then by citations
Cited by
Sorted by citations
A mesoscale connectome of the mouse brain
Oh, S. W., Harris, J. A., Ng, L., Winslow, B., Cain, N., Mihalas, S., Wang, Q., Lau, C., Kuan, L., Henry, A. M., et al. (2014) · Nature · doi:10.1038/nature13186 · Cited by 2,612 · see citing works
Self-citationThe Allen Mouse Brain Common Coordinate Framework: A 3D Reference Atlas
Wang, Q., Ding, S., Li, Y., Royall, J. J., Feng, D. H., Lesnar, P., Graddis, N., Naeemi, M., Facer, B. A. C., Ho, A., et al. (2020) · Cell · doi:10.1016/j.cell.2020.04.007 · Cited by 1,410 · see citing works
Self-citationWatakabe, A., Ohtsuka, M., Kinoshita, M., Takaji, M., Isa, K., Mizukami, H., Ozawa, K., Isa, T., & Yamamori, T. (2015) · Neuroscience Research · doi:10.1016/j.neures.2014.09.002 · Cited by 303 · see citing works
Gale, S. D., & Murphy, G. J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2768-14.2014 · Cited by 226 · see citing works
Gămănuț, R., Kennedy, H., Toroczkai, Z., Ercsey-Ravasz, M., Essen, D. C. V., Knoblauch, K., & Burkhalter, A. (2018) · Neuron · doi:10.1016/j.neuron.2017.12.037 · Cited by 202 · see citing works
Organization of the connections between claustrum and cortex in the mouse
Wang, Q., Ng, L., Harris, J. A., Feng, D. H., Li, Y., Royall, J. J., Oh, S. W., Bernard, A., Sunkin, S. M., Christof Koch, A., et al. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24047 · Cited by 197 · see citing works
Self-citationCommunication in Neural Circuits: Tools, Opportunities, and Challenges
Lerner, T. N., Ye, L., & Deisseroth, K. (2016) · Cell · doi:10.1016/j.cell.2016.02.027 · Cited by 159 · see citing works
Zhou, L., Liu, M., Li, Q., Deng, J., Mu, D., & Sun, Y.-G. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.077 · Cited by 116 · see citing works
Viral Vectors for Neural Circuit Mapping and Recent Advances in Trans-synaptic Anterograde Tracers
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 120 · see citing works
Neuroanatomical tract-tracing techniques that did go viral
Lanciego, J. L., & Wouterlood, F. G. (2020) · Brain Structure and Function · doi:10.1007/s00429-020-02041-6 · Cited by 100 · see citing works
Nguyen, H. N., Huppé‐Gourgues, F., & Vaucher, E. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00001 · Cited by 61 · see citing works
Albrecht, O., Dondzillo, A., Mayer, F., Thompson, J. A., & Klug, A. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00083 · Cited by 59 · see citing works
Aggleton, J. P., Yanakieva, S., Sengpiel, F., & Nelson, A. J. D. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107516 · Cited by 55 · see citing works
Hashimoto, M., Yamanaka, A., Kato, S., Tanifuji, M., Kobayashi, K., & Yaginuma, H. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00006 · Cited by 59 · see citing works
Wouterlood, F. G., Bloem, B., Mansvelder, H. D., Luchicchi, A., & Deisseroth, K. A. (2014) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2014.07.021 · Cited by 54 · see citing works
Two major network domains in the dorsal raphe nucleus
Commons, K. G. (2015) · Journal of Comparative Neurology · doi:10.1002/cne.23748 · Cited by 46 · see citing works
Corticofugal GABAergic projection neurons in the mouse frontal cortex
Tomioka, R., Sakimura, K., & Yanagawa, Y. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00133 · Cited by 44 · see citing works
Osanai, Y., Shimizu, T., Mori, T., Yoshimura, Y., Hatanaka, N., Nambu, A., Kimori, Y., Koyama, S., Kobayashi, K., & Ikenaka, K. (2016) · Glia · doi:10.1002/glia.23076 · Cited by 40 · see citing works
Wagener, R. J., Witte, M., Guy, J., Mingo-Moreno, N., Kügler, S., & Staiger, J. F. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv257 · Cited by 31 · see citing works
Watakabe, A., Takaji, M., Kato, S., Kobayashi, K., Mizukami, H., Ozawa, K., Ohsawa, S., Matsui, R., Watanabe, D., & Yamamori, T. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00110 · Cited by 28 · see citing works
Connectomic Analysis of Brain Networks: Novel Techniques and Future Directions
Cazemier, J. L., Clascá, F., & Tiesinga, P. H. E. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00110 · Cited by 27 · see citing works
Wang, J., & Zhang, L. (2021) · Microbes and Infection · doi:10.1016/j.micinf.2021.104829 · Cited by 23 · see citing works
A consideration of brain networks modulating social behavior
Kelly, A. M. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105138 · Cited by 24 · see citing works
Axonal Projections From the Middle Temporal Area in the Common Marmoset
Abe, H., Tani, T., Mashiko, H., Kitamura, N., Hayami, T., Watanabe, S., Sakai, K., Suzuki, W., Mizukami, H., Watakabe, A., et al. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00089 · Cited by 24 · see citing works
Use of Adeno‐Associated and Herpes Simplex Viral Vectors for In Vivo Neuronal Expression in Mice
Penrod, R. D., Wells, A. M., Carlezon, W. A., & Cowan, C. W. (2015) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0437s73 · Cited by 22 · see citing works
Okamoto, S., Yamauchi, K., Sohn, J., Takahashi, M., Ishida, Y., Furuta, T., Koike, M., Fujiyama, F., & Hioki, H. (2020) · STAR Protocols · doi:10.1016/j.xpro.2020.100230 · Cited by 21 · see citing works
Jaarsma, D., Blot, F. G. C., Wu, B., Venkatesan, S., Voogd, J., Meijer, D., Ruigrok, T. J. H., Gao, Z., Schonewille, M., & Zeeuw, C. I. D. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24479 · Cited by 14 · see citing works
Yamauchi, K., Okamoto, S., Ishida, Y., Konno, K., Hoshino, K., Furuta, T., Takahashi, M., Koike, M., Isa, K., Watanabe, M., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-19085-9 · Cited by 13 · see citing works
Oh, S. W., Son, S. J., Morris, J. A., Choi, J. H., Lee, C., & Rah, J. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa230 · Cited by 11 · see citing works
Self-citationReiten, I., Olsen, G. M., Bjaalie, J. G., Witter, M. P., & Leergaard, T. B. (2023) · Scientific Data · doi:10.1038/s41597-023-02527-y · Cited by 10 · see citing works
Zyuzin, J., & Jendzjowsky, N. G. (2022) · Journal of Neurophysiology · doi:10.1152/jn.00125.2022 · Cited by 7 · see citing works
Convergence Circuit Mapping: Genetic Approaches From Structure to Function
Yook, J. S., Kim, J., & Kim, J. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.688673 · Cited by 6 · see citing works
Johnson, B. A., & Frostig, R. D. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00050 · Cited by 6 · see citing works
Analyzing Thalamocortical Tract-Tracing Experiments in a Common Reference Space
Timonidis, N., Rubio-Teves, M., Alonso-Martínez, C., Bakker, R., García‐Amado, M., Tiesinga, P. H. E., & Clascá, F. (2023) · Neuroinformatics · doi:10.1007/s12021-023-09644-4 · Cited by 3 · see citing works
Negishi, K., Montes, L. P., Navarro, V. I., Arzate, L. S., Oliveros, C., & Khan, A. M. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.29.615708 · Cited by 2 · see citing works
A Guide to In Vivo Optogenetic Applications for Cerebellar Studies
Rooda, O. H. J. E., & Hoebeek, F. E. (2017) · Neuromethods · doi:10.1007/978-1-4939-7549-5_6 · Cited by 1 · see citing works
Anterograde Viral Tracer Methods
Beier, K. T. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801393-9.00010-4 · Cited by 1 · see citing works
Neuroanatomical Tracing Based on Selective Fluorochrome Expression in Transgenic Animals
Wouterlood, F. G. (2020) · Neuromethods · doi:10.1007/978-1-0716-0428-1_4 · Cited by 1 · see citing works
Major progress towards elucidating brain wiring diagrams
Rubenstein, J. L. R. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23586
Kobayashi-Sakashita, M., Lu, M.-H., Takeuchi, Y., Fendt, M., Uematsu, A., & Kiyokawa, Y. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.12.013
Optimizing stereotaxic injection strategy for AAV-mediated corticospinal tract tracing in mice
Wang, W., Zhang, T., Li, S., Wang, W., Jin, Q., Zhang, C., Liu, J., Sun, H., & Feng, S. (2026) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2026.110679
How does brain size influence the network properties of the cortex?
Gamanut, A. R. (2016) · theses.fr (ABES) · doi:10.70675/95831b16zc60cz4b46za557z4c90134677ea
AAV-delivered TurboRFP enables streamlined tracing and analysis of corticospinal tract sprouting
Hernaiz-Llorens, M., Londoño, C. J., Wang, E., Cai, F., Saikia, J. M., Chavez‐Martinez, C. L., Kim, H. J., Agba, C. K., & Zheng, B. (2026) · Cell Reports Methods · doi:10.1016/j.crmeth.2026.101540
Melichar, A., Suchankova, S., Rybalko, N., Pysanenko, K., Hruskova, B., Šuta, D., Dittrichová, J., Jovanović, N., Kozelková, K., Bettler, B., et al. (2026) · Neurobiology of Disease · doi:10.1016/j.nbd.2026.107664
- Authors
- Wang, Q., Henry, A. M., Harris, J. A., Oh, S. W., Joines, K. M., Nyhus, J., Hirokawa, K. E., Dee, N., Mortrud, M., Parry, S., Ouellette, B., Caldejon, S., Bernard, A., Jones, A. R., Zeng, H., & Hohmann, J. G.
- Affiliations
- Allen Institute for Brain Science (US)
- Corresponding author
- Hohmann, John G.
- ORCID
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2014-04-19
- Volume
- 522
- Issue
- 9
- Pages
- 1989-2012
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W1508489241
- Cited by
- 44
- References
- 94
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 1 · 2023: 2 · 2022: 3 · 2021: 3 · 2020: 6 · 2018: 5 · 2017: 2 · 2016: 6 · 2015: 5 · 2014: 7
- FWCI
- 4.37
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- adeno-associated virus, biotinylated dextran amine, primary motor cortex, primary somatosensory cortex, caudoputamen, retrograde tracing, neural circuits, mouse brain, iontophoresis
- MeSH terms
- Dependovirus, Animals, Biotin, Brain, Cell Count, Dextrans, Fluorescent Dyes, Immunohistochemistry, Mice, Inbred C57BL, Microscopy, Fluorescence, Neural Pathways, Neurons, Photomicrography, Sensitivity and Specificity, Microscopy, Confocal, Neuronal Tract-Tracers, Neuroanatomical Tract-Tracing Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review