{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T07:07:33Z","timestamp":1784704053312,"version":"3.55.0"},"reference-count":102,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T00:00:00Z","timestamp":1784678400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neural Circuits"],"abstract":"<jats:p>The application of transsynaptic viruses has transformed neural circuit analysis, enabling increasingly precise mapping of neuronal connectivity. These approaches can be broadly divided into polysynaptic and monosynaptic strategies. Polysynaptic retrograde tracers based on pseudorabies virus, including the classically selected Bartha strain and genetically engineered retrograde variants have provided important insights into multisynaptic circuit organization in rodents. For polysynaptic anterograde tracing, herpes simplex virus strain H129 and its derivatives have been used to map output pathways, with later genetic modifications improving detectability and experimental control. Over the past few years, growing attention has shifted toward monosynaptic tracing based on engineered rabies virus platforms used in combination with adeno-associated virus helper systems, which enable genetically restricted spread to direct presynaptic partners. Viral tracing is increasingly integrated with functional approaches, including calcium and voltage imaging, optogenetics, chemogenetics, and recombinase-based genetic strategies, thereby extending circuit analysis from anatomical mapping to causal interrogation of the function of defined neuronal populations. Looking forward, improved control of polysynaptic spread, together with large transgene capacity, suitability for tracing hierarchical circuit architecture, and the ability to incorporate functional readouts, is expected to revive interest in multisynaptic tracing.<\/jats:p>","DOI":"10.3389\/fncir.2026.1893057","type":"journal-article","created":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T06:33:04Z","timestamp":1784701984000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Transsynaptic viral tools in neural circuit analysis: from anatomical mapping to functional interrogation"],"prefix":"10.3389","volume":"20","author":[{"given":"Zsolt","family":"Boldogk\u0151i","sequence":"first","affiliation":[{"name":"Department of Medical Biology, Albert Szent-Gy\u00f6rgyi Medical School, University of Szeged","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"G\u00e1bor","family":"Torma","sequence":"additional","affiliation":[{"name":"Department of Medical Biology, Albert Szent-Gy\u00f6rgyi Medical School, University of Szeged","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zsolt","family":"Csabai","sequence":"additional","affiliation":[{"name":"Department of Medical Biology, Albert Szent-Gy\u00f6rgyi Medical School, University of Szeged","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zolt\u00e1n","family":"M\u00e1t\u00e9","sequence":"additional","affiliation":[{"name":"Medical Gene Technology Unit, HUN-REN Institute of Experimental Medicine","place":["Budapest, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rebeka","family":"Fekete","sequence":"additional","affiliation":[{"name":"Department of Medical Biology, Albert Szent-Gy\u00f6rgyi Medical School, University of Szeged","place":["Szeged, Hungary"]},{"name":"Laboratory of Neuroimmunology, HUN-REN Institute of Experimental Medicine","place":["Budapest, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M\u00e1t\u00e9","family":"Mizik","sequence":"additional","affiliation":[{"name":"Department of Medical Biology, Albert Szent-Gy\u00f6rgyi Medical School, University of Szeged","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ferenc","family":"Erd\u00e9lyi","sequence":"additional","affiliation":[{"name":"Medical Gene Technology Unit, HUN-REN Institute of Experimental Medicine","place":["Budapest, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"D\u00f3ra","family":"Tomb\u00e1cz","sequence":"additional","affiliation":[{"name":"Department of Medical Biology, Albert Szent-Gy\u00f6rgyi Medical School, University of Szeged","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"\u00c1d\u00e1m","family":"D\u00e9nes","sequence":"additional","affiliation":[{"name":"Laboratory of Neuroimmunology, HUN-REN Institute of Experimental Medicine","place":["Budapest, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,7,22]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.neuron.2009.06.014","article-title":"Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors","volume":"63","author":"Alexander","year":"2009","journal-title":"Neuron"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"732","DOI":"10.1038\/89522","article-title":"A neural circuit for circadian regulation of arousal","volume":"4","author":"Aston-Jones","year":"2001","journal-title":"Nat. Neurosci."},{"key":"ref3","first-page":"42","article-title":"Experiments to reduce the virulence of Aujeszky\u2019s virus","author":"Bartha","year":"1961","journal-title":"Magy. Allatorv. Lapja"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1016\/j.jchemneu.2019.05.001","article-title":"Hitchhiking on the neuronal highway: mechanisms of transsynaptic specificity","volume":"99","author":"Beier","year":"2019","journal-title":"J. Chem. Neuroanat."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"622","DOI":"10.1016\/j.cell.2015.07.015","article-title":"Circuit architecture of VTA dopamine neurons revealed by systematic input-output mapping","volume":"162","author":"Beier","year":"2015","journal-title":"Cell"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"7446","DOI":"10.1523\/JNEUROSCI.20-19-07446.2000","article-title":"Definition of neuronal circuitry controlling the activity of phrenic and abdominal motoneurons in the ferret using recombinant strains of pseudorabies virus","volume":"20","author":"Billig","year":"2000","journal-title":"J. Neurosci."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1038\/nmeth.1292","article-title":"Genetically timed, activity-sensor and rainbow transsynaptic viral tools","volume":"6","author":"Boldogkoi","year":"2009","journal-title":"Nat. Methods"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1002\/(SICI)1522-7243(199903\/04)14:2<>3.0.CO;2-B2","article-title":"Construction of a recombinant herpesvirus expressing the jellyfish green fluorescent protein","volume":"14","author":"Boldogk\u00f6i","year":"1999","journal-title":"Luminescence"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1016\/S0169-328X(02)00546-6","article-title":"Construction of recombinant pseudorabies viruses optimized for labeling and neurochemical characterization of neural circuitry","volume":"109","author":"Boldogk\u00f6i","year":"2002","journal-title":"Mol. Brain Res."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1016\/j.pneurobio.2004.03.010","article-title":"Novel tracing paradigms\u2014genetically engineered herpesviruses as tools for mapping functional circuits within the CNS: present status and future prospects","volume":"72","author":"Boldogk\u00f6i","year":"2004","journal-title":"Prog. Neurobiol."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"1951","DOI":"10.1038\/s41380-024-02451-6","article-title":"New rabies viral resources for multi-scale neural circuit mapping","volume":"29","author":"Bouin","year":"2024","journal-title":"Mol. Psychiatry"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"1263","DOI":"10.1038\/nn1525","article-title":"Millisecond-timescale, genetically targeted optical control of neural activity","volume":"8","author":"Boyden","year":"2005","journal-title":"Nat. Neurosci."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"388","DOI":"10.1016\/j.neuron.2016.02.038","article-title":"Morphological substrates for parallel streams of corticogeniculate feedback originating in both V1 and V2 of the macaque monkey","volume":"90","author":"Briggs","year":"2016","journal-title":"Neuron"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"8979","DOI":"10.1523\/JNEUROSCI.0409-15.2015","article-title":"Monosynaptic circuit tracing with glycoprotein-deleted rabies viruses","volume":"35","author":"Callaway","year":"2015","journal-title":"J. Neurosci."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"2515","DOI":"10.1523\/JNEUROSCI.13-06-02515.1993","article-title":"Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport, and pathogenesis","volume":"13","author":"Card","year":"1993","journal-title":"J. Neurosci."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"1974","DOI":"10.1523\/JNEUROSCI.10-06-01974.1990","article-title":"Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system","volume":"10","author":"Card","year":"1990","journal-title":"J. Neurosci."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1016\/j.neuron.2024.11.019","article-title":"A brain-wide map of descending inputs onto spinal V1 interneurons","volume":"113","author":"Chapman","year":"2025","journal-title":"Neuron"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"638","DOI":"10.1038\/s41593-018-0091-7","article-title":"Nontoxic, double-deletion-mutant rabies viral vectors for retrograde targeting of projection neurons","volume":"21","author":"Chatterjee","year":"2018","journal-title":"Nat. Neurosci."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"772","DOI":"10.1016\/j.cell.2019.09.023","article-title":"High-throughput mapping of long-range neuronal projection using in situ sequencing","volume":"179","author":"Chen","year":"2019","journal-title":"Cell"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1038\/nature12354","article-title":"Ultrasensitive fluorescent proteins for imaging neuronal activity","volume":"499","author":"Chen","year":"2013","journal-title":"Nature"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"332","DOI":"10.1038\/nature12107","article-title":"Structural and molecular interrogation of intact biological systems","volume":"497","author":"Chung","year":"2013","journal-title":"Nature"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"e83459","DOI":"10.7554\/eLife.83459","article-title":"Genomic stability of self-inactivating rabies","volume":"12","author":"Ciabatti","year":"2023","journal-title":"eLife"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"382","DOI":"10.1016\/j.cell.2017.06.014","article-title":"Life-long genetic and functional access to neural circuits using self-inactivating rabies virus","volume":"170","author":"Ciabatti","year":"2017","journal-title":"Cell"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"e1867232024","DOI":"10.1523\/JNEUROSCI.1867-23.2024","article-title":"Calretinin-expressing neurons in the basal forebrain specifically contact granule cells in the olfactory bulb and modulate Odor learning","volume":"45","author":"Constantinescu","year":"2025","journal-title":"J. Neurosci."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"135517","DOI":"10.1016\/j.neulet.2020.135517","article-title":"Pinealocytes can not transport neurotropic viruses. Pinealo-to-retinal connection in prepubertal rats originates from pineal neurons: light and electron microscopic immunohistochemical studies","volume":"744","author":"Cs\u00e1ki","year":"2021","journal-title":"Neurosci. Lett."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"1173","DOI":"10.1128\/JVI.02102-08","article-title":"Repair of the UL21 locus in pseudorabies virus Bartha enhances the kinetics of retrograde, Transneuronal infection in vitro and in vivo","volume":"83","author":"Curanovi\u0107","year":"2009","journal-title":"J. Virol."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1038\/s41592-019-0435-6","article-title":"High-performance calcium sensors for imaging activity in neuronal populations and microcompartments","volume":"16","author":"Dana","year":"2019","journal-title":"Nat. Methods"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"947","DOI":"10.1016\/j.neuroscience.2005.03.060","article-title":"Central autonomic control of the bone marrow: multisynaptic tract tracing by recombinant pseudorabies virus","volume":"134","author":"D\u00e9nes","year":"2005","journal-title":"Neuroscience"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"e01957-19","DOI":"10.1128\/JVI.01957-19","article-title":"Anterograde viral tracer herpes simplex virus 1 strain H129 transports primarily as capsids in cortical neuron axons","volume":"94","author":"Dong","year":"2020","journal-title":"J. Virol."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"6191","DOI":"10.1073\/pnas.93.12.6191","article-title":"Flp recombinase promotes site-specific DNA recombination in embryonic stem cells and transgenic mice","volume":"93","author":"Dymecki","year":"1996","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"603","DOI":"10.1016\/j.conb.2003.08.001","article-title":"Recent advances in the use of neurotropic viruses for circuit analysis","volume":"13","author":"Enquist","year":"2003","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"752","DOI":"10.1006\/bbrc.1997.7124","article-title":"Regulation of Cre recombinase activity by mutated Estrogen receptor ligand-binding domains","volume":"237","author":"Feil","year":"1997","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"461","DOI":"10.1007\/s00401-018-1885-0","article-title":"Microglia control the spread of neurotropic virus infection via P2Y12 signalling and recruit monocytes through P2Y12-independent mechanisms","volume":"136","author":"Fekete","year":"2018","journal-title":"Acta Neuropathol."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"763","DOI":"10.1038\/nmeth.2996","article-title":"Targeting cells with single vectors using multiple-feature Boolean logic","volume":"11","author":"Fenno","year":"2014","journal-title":"Nat. Methods"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"584","DOI":"10.1002\/cne.25451","article-title":"Monosynaptic restriction of the anterograde herpes simplex virus strain H129 for neural circuit tracing","volume":"531","author":"Fischer","year":"2023","journal-title":"J. Comp. Neurol."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"3417","DOI":"10.1038\/s41467-022-31072-2","article-title":"Brain-wide reconstruction of inhibitory circuits after traumatic brain injury","volume":"13","author":"Frankowski","year":"2022","journal-title":"Nat. Commun."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1159\/000054372","article-title":"Neuronal Labeling in the rat brain and spinal cord from the ovary using viral transneuronal tracing technique","volume":"68","author":"Gerendai","year":"1998","journal-title":"Neuroendocrinology"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"1361","DOI":"10.1126\/science.aab0810","article-title":"High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor","volume":"350","author":"Gong","year":"2015","journal-title":"Science"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"5547","DOI":"10.1073\/pnas.89.12.5547","article-title":"Tight control of gene expression in mammalian cells by tetracycline-responsive promoters","volume":"89","author":"Gossen","year":"1992","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"e6923","DOI":"10.1371\/journal.pone.0006923","article-title":"Fluorescence-based monitoring of in vivo neural activity using a circuit-tracing pseudorabies virus","volume":"4","author":"Granstedt","year":"2009","journal-title":"PLoS One"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"773","DOI":"10.1016\/j.neuron.2013.03.025","article-title":"Permanent genetic access to transiently active neurons via TRAP: targeted recombination in active populations","volume":"78","author":"Guenthner","year":"2013","journal-title":"Neuron"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"3455","DOI":"10.1038\/s41467-024-47966-2","article-title":"Synergism between two BLA-to-BNST pathways for appropriate expression of anxiety-like behaviors in male mice","volume":"15","author":"Han","year":"2024","journal-title":"Nat. Commun."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"937","DOI":"10.1046\/j.1460-9568.2002.01923.x","article-title":"Oestrogen-dependent tracing in the rat CNS after pseudorabies virus infection","volume":"15","author":"Horv\u00e1th","year":"2002","journal-title":"Eur. J. Neurosci."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"e2023481120","DOI":"10.1073\/pnas.2023481120","article-title":"\u201cSelf-inactivating\u201d rabies viruses are susceptible to loss of their intended attenuating modification","volume":"120","author":"Jin","year":"2023","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1038\/s41593-023-01545-8","article-title":"Long-term labeling and imaging of synaptically connected neuronal networks in vivo using double-deletion-mutant rabies viruses","volume":"27","author":"Jin","year":"2024","journal-title":"Nat. Neurosci."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"975","DOI":"10.1016\/j.neuron.2016.07.036","article-title":"High-throughput mapping of single-neuron projections by sequencing of barcoded RNA","volume":"91","author":"Kebschull","year":"2016","journal-title":"Neuron"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"4657","DOI":"10.1523\/JNEUROSCI.23-11-04657.2003","article-title":"Brainstem substrates of sympatho-motor circuitry identified using trans-synaptic tracing with pseudorabies virus recombinants","volume":"23","author":"Kerman","year":"2003","journal-title":"J. Neurosci."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"719","DOI":"10.1038\/s41583-019-0231-4","article-title":"Optical voltage imaging in neurons: moving from technology development to practical tool","volume":"20","author":"Kn\u00f6pfel","year":"2019","journal-title":"Nat. Rev. Neurosci."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"806","DOI":"10.1016\/j.chom.2012.10.013","article-title":"Kinesin-3 mediates axonal sorting and directional transport of alphaherpesvirus particles in neurons","volume":"12","author":"Kramer","year":"2012","journal-title":"Cell Host Microbe"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"9431","DOI":"10.1128\/JVI.01317-13","article-title":"Glycoproteins gE and gI are required for efficient KIF1A-dependent anterograde axonal transport of alphaherpesvirus particles in neurons","volume":"87","author":"Kratchmarov","year":"2013","journal-title":"J. Virol."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"938","DOI":"10.1016\/j.neuron.2011.12.002","article-title":"A Cre-dependent, anterograde transsynaptic viral tracer for mapping output pathways of genetically marked neurons","volume":"72","author":"Lo","year":"2011","journal-title":"Neuron"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"11363","DOI":"10.1128\/JVI.01281-07","article-title":"Pseudorabies virus Us9 directs axonal sorting of viral capsids","volume":"81","author":"Lyman","year":"2007","journal-title":"J. Virol."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1016\/j.neuron.2010.01.003","article-title":"A Disynaptic relay from superior colliculus to dorsal stream visual cortex in macaque monkey","volume":"65","author":"Lyon","year":"2010","journal-title":"Neuron"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"867","DOI":"10.1016\/0361-9230(89)90032-4","article-title":"Golgi-like, transneuronal retrograde labelling with CNS injections of herpes simplex virus type","volume":"22","author":"McLean","year":"1989","journal-title":"Brain Res. Bull."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"882","DOI":"10.1038\/42264","article-title":"Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin","volume":"388","author":"Miyawaki","year":"1997","journal-title":"Nature"},{"key":"ref56","doi-asserted-by":"publisher","first-page":"5370","DOI":"10.1523\/JNEUROSCI.1219-04.2004","article-title":"Identification of sympathetic premotor neurons in medullary raphe regions mediating fever and other thermoregulatory functions","volume":"24","author":"Nakamura","year":"2004","journal-title":"J. Neurosci."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"12789","DOI":"10.1523\/JNEUROSCI.4044-06.2006","article-title":"Multiple circuits relaying primate parallel visual pathways to the middle temporal area","volume":"26","author":"Nassi","year":"2006","journal-title":"J. Neurosci."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1038\/nature13186","article-title":"A mesoscale connectome of the mouse brain","volume":"508","author":"Oh","year":"2014","journal-title":"Nature"},{"key":"ref59","doi-asserted-by":"publisher","first-page":"617","DOI":"10.1016\/j.neuron.2011.07.005","article-title":"New rabies virus variants for monitoring and manipulating activity and gene expression in defined neural circuits","volume":"71","author":"Osakada","year":"2011","journal-title":"Neuron"},{"key":"ref60","doi-asserted-by":"publisher","first-page":"e89297","DOI":"10.7554\/eLife.89297","article-title":"Postsynaptic cell type and synaptic distance do not determine efficiency of monosynaptic rabies virus spread measured at synaptic resolution","volume":"12","author":"Pati\u00f1o","year":"","journal-title":"eLife"},{"key":"ref61","doi-asserted-by":"publisher","first-page":"e2203677119","DOI":"10.1073\/pnas.2203677119","article-title":"Single-cell transcriptomic classification of rabies-infected cortical neurons","volume":"119","author":"Pati\u00f1o","year":"","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"3851","DOI":"10.1016\/j.neuron.2024.09.003","article-title":"Transcriptomic cell-type specificity of local cortical circuits","volume":"112","author":"Pati\u00f1o","year":"2024","journal-title":"Neuron"},{"key":"ref63","doi-asserted-by":"publisher","first-page":"2701","DOI":"10.1523\/JNEUROSCI.22-07-02701.2002","article-title":"Intravitreal injection of the attenuated pseudorabies virus PRV Bartha results in infection of the Hamster suprachiasmatic nucleus only by retrograde transsynaptic transport via autonomic circuits","volume":"22","author":"Pickard","year":"2002","journal-title":"J. Neurosci."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"109721","DOI":"10.1016\/j.celrep.2021.109721","article-title":"Homologous organization of cerebellar pathways to sensory, motor, and associative forebrain","volume":"36","author":"Pisano","year":"2021","journal-title":"Cell Rep."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"462","DOI":"10.1128\/MMBR.69.3.462-500.2005","article-title":"Molecular biology of pseudorabies virus: impact on neurovirology and veterinary medicine","volume":"69","author":"Pomeranz","year":"2005","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"711","DOI":"10.1016\/j.neuron.2016.01.004","article-title":"Rabies virus CVS-N2c \u0394G strain enhances retrograde synaptic transfer and neuronal viability","volume":"89","author":"Reardon","year":"2016","journal-title":"Neuron"},{"key":"ref67","doi-asserted-by":"publisher","first-page":"896","DOI":"10.1016\/j.cell.2014.10.010","article-title":"iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging","volume":"159","author":"Renier","year":"2014","journal-title":"Cell"},{"key":"ref68","doi-asserted-by":"publisher","first-page":"2731","DOI":"10.1523\/JNEUROSCI.20-07-02731.2000","article-title":"Progressive postnatal assembly of limbic-autonomic circuits revealed by central transneuronal transport of pseudorabies virus","volume":"20","author":"Rinaman","year":"2000","journal-title":"J. Neurosci."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1016\/S0165-3806(99)00039-5","article-title":"Retrograde transynaptic pseudorabies virus infection of central autonomic circuits in neonatal rats","volume":"114","author":"Rinaman","year":"1999","journal-title":"Dev. Brain Res."},{"key":"ref70","doi-asserted-by":"publisher","first-page":"1101","DOI":"10.1038\/s41592-025-02670-x","article-title":"ATLAS: a rationally designed anterograde transsynaptic tracer","volume":"22","author":"Rivera","year":"2025","journal-title":"Nat. Methods"},{"key":"ref71","doi-asserted-by":"publisher","first-page":"109005","DOI":"10.1016\/j.jneumeth.2020.109005","article-title":"Can transsynaptic viral strategies be used to reveal functional aspects of neural circuitry?","volume":"348","author":"Rogers","year":"2021","journal-title":"J. Neurosci. Methods"},{"key":"ref72","doi-asserted-by":"publisher","first-page":"739","DOI":"10.1016\/j.neuron.2016.10.015","article-title":"Capturing and manipulating activated neuronal ensembles with CANE delineates a hypothalamic social-fear circuit","volume":"92","author":"Sakurai","year":"2016","journal-title":"Neuron"},{"key":"ref73","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1038\/s41586-023-06570-y","article-title":"Transcriptional linkage analysis with in vivo AAV-perturb-seq","volume":"622","author":"Santinha","year":"2023","journal-title":"Nature"},{"key":"ref74","doi-asserted-by":"publisher","first-page":"5166","DOI":"10.1073\/pnas.85.14.5166","article-title":"Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1","volume":"85","author":"Sauer","year":"1988","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref75","doi-asserted-by":"publisher","first-page":"6993","DOI":"10.1038\/s41467-022-34334-1","article-title":"Ascertaining cells\u2019 synaptic connections and RNA expression simultaneously with barcoded rabies virus libraries","volume":"13","author":"Saunders","year":"2022","journal-title":"Nat. Commun."},{"key":"ref76","doi-asserted-by":"publisher","first-page":"e1007985","DOI":"10.1371\/journal.ppat.1007985","article-title":"A kinesin-3 recruitment complex facilitates axonal sorting of enveloped alpha herpesvirus capsids","volume":"16","author":"Scherer","year":"2020","journal-title":"PLoS Pathog."},{"key":"ref77","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1038\/nature14600","article-title":"Viral-genetic tracing of the input\u2013output organization of a central noradrenaline circuit","volume":"524","author":"Schwarz","year":"2015","journal-title":"Nature"},{"key":"ref78","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1002\/cne.20921","article-title":"Selective spread of neurotropic herpesviruses in the rat hippocampus","volume":"496","author":"S\u00edk","year":"2006","journal-title":"J. Comp. Neurol."},{"key":"ref79","doi-asserted-by":"publisher","first-page":"9264","DOI":"10.1073\/pnas.97.16.9264","article-title":"Pseudorabies virus expressing enhanced green fluorescent protein: a tool for in vitro electrophysiological analysis of transsynaptically labeled neurons in identified central nervous system circuits","volume":"97","author":"Smith","year":"2000","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref80","doi-asserted-by":"publisher","first-page":"274","DOI":"10.1016\/0006-8993(89)90063-2","article-title":"CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labelling with pseudorabies virus","volume":"491","author":"Strack","year":"1989","journal-title":"Brain Res."},{"key":"ref81","doi-asserted-by":"publisher","first-page":"5405","DOI":"10.1128\/jvi.70.8.5405-5413.1996","article-title":"Anterograde, transneuronal transport of herpes simplex virus type 1 strain H129 in the murine visual system","volume":"70","author":"Sun","year":"1996","journal-title":"J. Virol."},{"key":"ref82","doi-asserted-by":"publisher","first-page":"783","DOI":"10.1016\/j.neuron.2017.10.011","article-title":"Transsynaptic mapping of second-order taste neurons in flies by trans-tango","volume":"96","author":"Talay","year":"2017","journal-title":"Neuron"},{"key":"ref83","doi-asserted-by":"publisher","first-page":"372","DOI":"10.1016\/j.neuron.2016.09.021","article-title":"A designer AAV variant permits efficient retrograde access to projection neurons","volume":"92","author":"Tervo","year":"2016","journal-title":"Neuron"},{"key":"ref84","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1007\/s11064-005-9018-2","article-title":"Serotonin-synthesizing neurons in the rostral medullary Raph\u00e9\/Parapyramidal region transneuronally labelled after injection of pseudorabies virus into the rat tail","volume":"31","author":"T\u00f3th","year":"2006","journal-title":"Neurochem. Res."},{"key":"ref85","doi-asserted-by":"publisher","first-page":"e0278053","DOI":"10.1371\/journal.pone.0278053","article-title":"Quantitative analysis of rabies virus-based synaptic connectivity tracing","volume":"18","author":"Tran-Van-Minh","year":"2023","journal-title":"PLoS One"},{"key":"ref86","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1016\/0006-8993(87)90931-0","article-title":"Retrograde transneuronal transfer of herpes simplex virus type 1 (HSV 1) from motoneurones","volume":"422","author":"Ugolini","year":"1987","journal-title":"Brain Res."},{"key":"ref87","doi-asserted-by":"publisher","first-page":"981","DOI":"10.1016\/j.cub.2007.04.058","article-title":"Local retinal circuits of melanopsin-containing ganglion cells identified by transsynaptic viral tracing","volume":"17","author":"Viney","year":"2007","journal-title":"Curr. Biol."},{"key":"ref88","doi-asserted-by":"publisher","first-page":"4000","DOI":"10.1523\/JNEUROSCI.3967-15.2016","article-title":"Brain-wide maps of synaptic input to cortical interneurons","volume":"36","author":"Wall","year":"2016","journal-title":"J. Neurosci."},{"key":"ref89","doi-asserted-by":"publisher","first-page":"21848","DOI":"10.1073\/pnas.1011756107","article-title":"Monosynaptic circuit tracing in vivo through Cre-dependent targeting and complementation of modified rabies virus","volume":"107","author":"Wall","year":"2010","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref90","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1038\/nmeth999","article-title":"Retrograde neuronal tracing with a deletion-mutant rabies virus","volume":"4","author":"Wickersham","year":"","journal-title":"Nat. Methods"},{"key":"ref91","doi-asserted-by":"publisher","first-page":"639","DOI":"10.1016\/j.neuron.2007.01.033","article-title":"Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons","volume":"53","author":"Wickersham","year":"","journal-title":"Neuron"},{"key":"ref92","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1038\/nprot.2009.248","article-title":"Production of glycoprotein-deleted rabies viruses for monosynaptic tracing and high-level gene expression in neurons","volume":"5","author":"Wickersham","year":"2010","journal-title":"Nat. Protoc."},{"key":"ref93","doi-asserted-by":"publisher","first-page":"1395","DOI":"10.1007\/s00429-014-0733-9","article-title":"The neuroinvasive profiles of H129 (herpes simplex virus type 1) recombinants with putative anterograde-only transneuronal spread properties","volume":"220","author":"Wojaczynski","year":"2015","journal-title":"Brain Struct. Funct."},{"key":"ref94","doi-asserted-by":"publisher","first-page":"e01850-14","DOI":"10.1128\/mBio.01850-14","article-title":"Characterization of a replication-incompetent pseudorabies virus mutant lacking the sole immediate early gene IE180","volume":"5","author":"Wu","year":"2014","journal-title":"mBio"},{"key":"ref95","doi-asserted-by":"publisher","first-page":"7645","DOI":"10.1038\/s41467-022-35355-6","article-title":"An HSV-1-H129 amplicon tracer system for rapid and efficient monosynaptic anterograde neural circuit tracing","volume":"13","author":"Xiong","year":"2022","journal-title":"Nat. Commun."},{"key":"ref96","doi-asserted-by":"publisher","first-page":"1029","DOI":"10.1016\/j.neuron.2020.07.010","article-title":"Viral vectors for neural circuit mapping and recent advances in trans-synaptic anterograde tracers","volume":"107","author":"Xu","year":"2020","journal-title":"Neuron"},{"key":"ref97","doi-asserted-by":"publisher","first-page":"6759","DOI":"10.1523\/JNEUROSCI.23-17-06759.2003","article-title":"Reversible suppression of glutamatergic neurotransmission of cerebellar granule cells in vivo by genetically manipulated expression of tetanus neurotoxin light chain","volume":"23","author":"Yamamoto","year":"2003","journal-title":"J. Neurosci."},{"key":"ref98","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1186\/s13024-017-0179-7","article-title":"Anterograde monosynaptic transneuronal tracers derived from herpes simplex virus 1 strain H129","volume":"12","author":"Zeng","year":"2017","journal-title":"Mol. Neurodegener."},{"key":"ref99","doi-asserted-by":"publisher","first-page":"RP87866","DOI":"10.7554\/eLife.87866","article-title":"Rabies virus-based barcoded neuroanatomy resolved by single-cell RNA and in situ sequencing","volume":"12","author":"Zhang","year":"2024","journal-title":"eLife"},{"key":"ref100","doi-asserted-by":"publisher","first-page":"884","DOI":"10.1038\/s41586-023-05828-9","article-title":"Fast and sensitive GCaMP calcium indicators for imaging neural populations","volume":"615","author":"Zhang","year":"2023","journal-title":"Nature"},{"key":"ref101","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/j.neuron.2016.11.045","article-title":"AAV-mediated anterograde transsynaptic tagging: mapping Corticocollicular input-defined neural pathways for Defense Behaviors","volume":"93","author":"Zingg","year":"2017","journal-title":"Neuron"},{"key":"ref102","doi-asserted-by":"publisher","first-page":"3250","DOI":"10.1523\/JNEUROSCI.2158-19.2020","article-title":"Synaptic specificity and application of anterograde transsynaptic AAV for probing neural circuitry","volume":"40","author":"Zingg","year":"2020","journal-title":"J. Neurosci."}],"container-title":["Frontiers in Neural Circuits"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncir.2026.1893057\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T06:33:06Z","timestamp":1784701986000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncir.2026.1893057\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,22]]},"references-count":102,"alternative-id":["10.3389\/fncir.2026.1893057"],"URL":"https:\/\/doi.org\/10.3389\/fncir.2026.1893057","relation":{},"ISSN":["1662-5110"],"issn-type":[{"value":"1662-5110","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,22]]},"article-number":"1893057"}}