{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,28]],"date-time":"2026-02-28T08:08:14Z","timestamp":1772266094673,"version":"3.50.1"},"reference-count":43,"publisher":"eLife Sciences Publications, Ltd","license":[{"start":{"date-parts":[[2017,2,3]],"date-time":"2017-02-03T00:00:00Z","timestamp":1486080000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2017,2,3]],"date-time":"2017-02-03T00:00:00Z","timestamp":1486080000000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2017,2,3]],"date-time":"2017-02-03T00:00:00Z","timestamp":1486080000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000065","name":"National Institute of Neurological Disorders and Stroke","doi-asserted-by":"publisher","award":["5R01NS020364-28"],"award-info":[{"award-number":["5R01NS020364-28"]}],"id":[{"id":"10.13039\/100000065","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000324","name":"Gatsby Charitable Foundation","doi-asserted-by":"publisher","award":["FONDECYT #1160888"],"award-info":[{"award-number":["FONDECYT #1160888"]}],"id":[{"id":"10.13039\/501100000324","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000025","name":"National Institute of Mental Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000025","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Conte Center, Harvard University","award":["1P50MH094271-01"],"award-info":[{"award-number":["1P50MH094271-01"]}]},{"DOI":"10.13039\/100000050","name":"National Heart, Lung, and Blood Institute","doi-asserted-by":"publisher","award":["5T32HL110852-03"],"award-info":[{"award-number":["5T32HL110852-03"]}],"id":[{"id":"10.13039\/100000050","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002850","name":"Fondo Nacional de Desarrollo Cient\u00edfico y Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["1160888"],"award-info":[{"award-number":["1160888"]}],"id":[{"id":"10.13039\/501100002850","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>In many parts of the nervous system, signals pass across multiple synaptic relays on their way to a destination, but little is known about how these relays form and the function they serve. To get some insight into this question we ask how the connectivity patterns are organized at two successive synaptic relays in a simple, cholinergic efferent pathway. We found that the organization at successive relays in the parasympathetic nervous system strongly resemble each other despite the different embryological origin and physiological properties of the pre- and postsynaptic cells. Additionally, we found a similar developmental synaptic pruning and elaboration strategy is used at both sites to generate their adult organizations. The striking parallels in adult innervation and developmental mechanisms at the relays argue that a general strategy is in operation. We discuss why from a functional standpoint this structural organization may amplify central signals while at the same time maintaining positional targeting.<\/jats:p>","DOI":"10.7554\/elife.23193","type":"journal-article","created":{"date-parts":[[2017,2,3]],"date-time":"2017-02-03T08:00:10Z","timestamp":1486108810000},"source":"Crossref","is-referenced-by-count":11,"title":["Similar synapse elimination motifs at successive relays in the same efferent pathway during development in mice"],"prefix":"10.7554","volume":"6","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0758-4654","authenticated-orcid":true,"given":"Shu-Hsien","family":"Sheu","sequence":"first","affiliation":[{"name":"Center for Brain Science, Harvard University, Cambridge, United States"},{"name":"Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Juan Carlos","family":"Tapia","sequence":"additional","affiliation":[{"name":"Center for Brain Science, Harvard University, Cambridge, United States"},{"name":"Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shlomo","family":"Tsuriel","sequence":"additional","affiliation":[{"name":"Center for Brain Science, Harvard University, Cambridge, United States"},{"name":"Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0208-3212","authenticated-orcid":true,"given":"Jeff W","family":"Lichtman","sequence":"additional","affiliation":[{"name":"Center for Brain Science, Harvard University, Cambridge, United States"},{"name":"Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"4374","published-online":{"date-parts":[[2017,2,3]]},"reference":[{"key":"bib1","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1113\/jphysiol.1967.sp008360","article-title":"The neural mechanism of binocular depth discrimination","volume":"193","author":"Barlow","year":"1967","journal-title":"The Journal of Physiology"},{"key":"bib2","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1038\/nature10532","article-title":"The evolution of gene expression levels in mammalian organs","volume":"478","author":"Brawand","year":"2011","journal-title":"Nature"},{"key":"bib3","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1113\/jphysiol.1976.sp011565","article-title":"Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation","volume":"261","author":"Brown","year":"1976","journal-title":"The Journal of Physiology"},{"key":"bib4","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1038\/nmeth.2450","article-title":"Improved tools for the brainbow toolbox","volume":"10","author":"Cai","year":"2013","journal-title":"Nature Methods"},{"key":"bib5","doi-asserted-by":"publisher","first-page":"e38011","DOI":"10.1371\/journal.pone.0038011","article-title":"TrakEM2 software for neural circuit reconstruction","volume":"7","author":"Cardona","year":"2012","journal-title":"PLoS One"},{"key":"bib6","doi-asserted-by":"publisher","first-page":"955","DOI":"10.1016\/S0896-6273(00)00166-5","article-title":"Developmental remodeling of the retinogeniculate synapse","volume":"28","author":"Chen","year":"2000","journal-title":"Neuron"},{"key":"bib7","doi-asserted-by":"publisher","first-page":"214","DOI":"10.1002\/neu.20022","article-title":"Age-associated synapse elimination in mouse parasympathetic ganglia","volume":"60","author":"Coggan","year":"2004","journal-title":"Journal of Neurobiology"},{"key":"bib8","doi-asserted-by":"publisher","first-page":"639","DOI":"10.1126\/science.309179","article-title":"Eye-specific termination bands in tecta of three-eyed frogs","volume":"202","author":"Constantine-Paton","year":"1978","journal-title":"Science"},{"key":"bib9","doi-asserted-by":"publisher","first-page":"694","DOI":"10.1038\/76649","article-title":"Competition at silent synapses in reinnervated skeletal muscle","volume":"3","author":"Costanzo","year":"2000","journal-title":"Nature Neuroscience"},{"key":"bib10","isbn-type":"print","volume-title":"Glandular Mechanisms of Salivary Secretion (Frontiers of Oral Biology , Vol. 10)","author":"Ekstrom","year":"1998","ISBN":"https:\/\/id.crossref.org\/isbn\/9783805566308"},{"key":"bib11","isbn-type":"print","volume-title":"Neural Mechanisms of Salivary Gland Secretion (Frontiers of Oral Biology, Vol. 11)","author":"Ekstrom","year":"1999","ISBN":"https:\/\/id.crossref.org\/isbn\/9783805568807"},{"key":"bib12","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1126\/science.1253286","article-title":"Neurodevelopment. parasympathetic ganglia derive from schwann cell precursors","volume":"345","author":"Espinosa-Medina","year":"2014","journal-title":"Science"},{"key":"bib13","doi-asserted-by":"publisher","first-page":"2327","DOI":"10.1111\/j.1460-9568.2009.06779.x","article-title":"On the mechanism of action of muscle fibre activity in synapse competition and elimination at the mammalian neuromuscular junction","volume":"29","author":"Favero","year":"2009","journal-title":"European Journal of Neuroscience"},{"key":"bib14","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/S0896-6273(00)00084-2","article-title":"Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP","volume":"28","author":"Feng","year":"2000","journal-title":"Neuron"},{"key":"bib15","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/0006-8993(81)90098-6","article-title":"Retinotopic analysis of fiber pathways in the regenerating retinotectal system of the adult newt Cynops pyrrhogaster","volume":"206","author":"Fujisawa","year":"1981","journal-title":"Brain Research"},{"key":"bib16","doi-asserted-by":"publisher","first-page":"1508","DOI":"10.1126\/science.282.5393.1508","article-title":"Synaptic segregation at the developing neuromuscular junction","volume":"282","author":"Gan","year":"1998","journal-title":"Science"},{"key":"bib17","doi-asserted-by":"publisher","first-page":"4667","DOI":"10.1007\/s00018-013-1405-2","article-title":"Synapse elimination in the developing cerebellum","volume":"70","author":"Hashimoto","year":"2013","journal-title":"Cellular and Molecular Life Sciences"},{"key":"bib18","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1016\/S0003-9969(99)00128-4","article-title":"Expression of connexin 32 and 43 in developing rat submandibular salivary glands","volume":"45","author":"Ihara","year":"2000","journal-title":"Archives of Oral Biology"},{"key":"bib19","doi-asserted-by":"publisher","first-page":"3151","DOI":"10.1113\/jphysiol.2012.248252","article-title":"Calcium-dependent regulation of climbing fibre synapse elimination during postnatal cerebellar development","volume":"591","author":"Kano","year":"2013","journal-title":"The Journal of Physiology"},{"key":"bib20","doi-asserted-by":"publisher","first-page":"648","DOI":"10.1016\/j.cell.2015.06.054","article-title":"Saturated reconstruction of a volume of neocortex","volume":"162","author":"Kasthuri","year":"2015","journal-title":"Cell"},{"key":"bib21","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1083\/jcb.79.1.20","article-title":"Physiological and morphological evidence for coupling in mouse salivary gland acinar cells","volume":"79","author":"Kater","year":"1978","journal-title":"The Journal of Cell Biology"},{"key":"bib22","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1152\/jn.00650.2003","article-title":"Common input to motor neurons innervating the same and different compartments of the human extensor digitorum muscle","volume":"91","author":"Keen","year":"2004","journal-title":"Journal of Neurophysiology"},{"key":"bib23","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1016\/S0896-6273(01)00383-X","article-title":"Asynchronous synapse elimination in neonatal motor units: studies using GFP transgenic mice","volume":"31","author":"Keller-Peck","year":"2001","journal-title":"Neuron"},{"key":"bib24","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1016\/S0896-6273(00)80893-4","article-title":"Synapse elimination and indelible memory","volume":"25","author":"Lichtman","year":"2000","journal-title":"Neuron"},{"key":"bib25","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/314357a0","article-title":"Multiple innervation of tonic endplates revealed by activity-dependent uptake of fluorescent probes","volume":"314","author":"Lichtman","year":"1985","journal-title":"Nature"},{"key":"bib26","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1113\/jphysiol.1977.sp012087","article-title":"The reorganization of synaptic connexions in the rat submandibular ganglion during post-natal development","volume":"273","author":"Lichtman","year":"1977","journal-title":"The Journal of Physiology"},{"key":"bib27","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1113\/jphysiol.1980.sp013233","article-title":"On the predominantly single innervation of submandibular ganglion cells in the rat","volume":"302","author":"Lichtman","year":"1980","journal-title":"The Journal of Physiology"},{"key":"bib28","doi-asserted-by":"publisher","first-page":"1093","DOI":"10.1369\/jhc.2008.951780","article-title":"Distribution of tight junction proteins in adult human salivary glands","volume":"56","author":"Maria","year":"2008","journal-title":"Journal of Histochemistry & Cytochemistry"},{"key":"bib29","doi-asserted-by":"publisher","first-page":"760","DOI":"10.1002\/dneu.20621","article-title":"In vivo imaging of presynaptic terminals and postsynaptic sites in the mouse submandibular ganglion","volume":"68","author":"McCann","year":"2008","journal-title":"Developmental Neurobiology"},{"key":"bib30","first-page":"477","volume-title":"Major Salivary Glands, in Histology for Pathologists","author":"Mills","year":"2012"},{"key":"bib31","volume-title":"Principles of Neural Development","author":"Purves","year":"1985"},{"key":"bib32","doi-asserted-by":"publisher","first-page":"804","DOI":"10.1016\/j.cub.2005.03.048","article-title":"Repulsive interactions shape the morphologies and functional arrangement of zebrafish peripheral sensory arbors","volume":"15","author":"Sagasti","year":"2005","journal-title":"Current Biology"},{"key":"bib33","doi-asserted-by":"publisher","first-page":"745","DOI":"10.1016\/0896-6273(90)90333-B","article-title":"Impulse activity and the patterning of connections during CNS development","volume":"5","author":"Shatz","year":"1990","journal-title":"Neuron"},{"key":"bib34","doi-asserted-by":"publisher","first-page":"602","DOI":"10.1073\/pnas.93.2.602","article-title":"Emergence of order in visual system development","volume":"93","author":"Shatz","year":"1996","journal-title":"PNAS"},{"key":"bib35","doi-asserted-by":"crossref","first-page":"1760","DOI":"10.1523\/JNEUROSCI.07-06-01760.1987","article-title":"The dendritic complexity and innervation of submandibular neurons in five species of mammals","volume":"7","author":"Snider","year":"1987","journal-title":"Journal of Neuroscience"},{"key":"bib36","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1016\/b978-0-12-385870-2.00019-6","volume-title":"Fundamental Neuroscience","author":"Tapia","year":"2013"},{"key":"bib37","doi-asserted-by":"publisher","first-page":"816","DOI":"10.1016\/j.neuron.2012.04.017","article-title":"Pervasive synaptic branch removal in the mammalian neuromuscular system at birth","volume":"74","author":"Tapia","year":"2012","journal-title":"Neuron"},{"key":"bib38","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1007\/BF00233608","article-title":"Gap junctions on myoepithelial cells","volume":"206","author":"Taugner","year":"1980","journal-title":"Cell and Tissue Research"},{"key":"bib39","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1016\/j.cell.2013.06.031","article-title":"Stacked endoplasmic reticulum sheets are connected by helicoidal membrane motifs","volume":"154","author":"Terasaki","year":"2013","journal-title":"Cell"},{"key":"bib40","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1038\/nmeth.3367","article-title":"Multispectral labeling technique to map many neighboring axonal projections in the same tissue","volume":"12","author":"Tsuriel","year":"2015","journal-title":"Nature Methods"},{"key":"bib41","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1126\/science.179.4071.395","article-title":"Somatosensory cortex: structural alterations following early injury to sense organs","volume":"179","author":"Van der Loos","year":"1973","journal-title":"Science"},{"key":"bib42","doi-asserted-by":"crossref","first-page":"4310","DOI":"10.1523\/JNEUROSCI.21-12-04310.2001","article-title":"Unique functional properties of on and off pathways in the developing mammalian retina","volume":"21","author":"Wang","year":"2001","journal-title":"Journal of Neuroscience"},{"key":"bib43","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1152\/jn.1965.28.6.1029","article-title":"Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens","volume":"28","author":"Wiesel","year":"1965","journal-title":"Journal of Neurophysiology"}],"container-title":["eLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/cdn.elifesciences.org\/articles\/23193\/elife-23193-v2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/cdn.elifesciences.org\/articles\/23193\/elife-23193-v2.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/elifesciences.org\/articles\/23193","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,11]],"date-time":"2023-10-11T20:49:49Z","timestamp":1697057389000},"score":1,"resource":{"primary":{"URL":"https:\/\/elifesciences.org\/articles\/23193"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,2,3]]},"references-count":43,"alternative-id":["10.7554\/eLife.23193"],"URL":"https:\/\/doi.org\/10.7554\/elife.23193","archive":["CLOCKSS"],"relation":{"has-review":[{"id-type":"doi","id":"10.7554\/eLife.23193.017","asserted-by":"object"},{"id-type":"doi","id":"10.7554\/eLife.23193.018","asserted-by":"object"}]},"ISSN":["2050-084X"],"issn-type":[{"value":"2050-084X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,2,3]]},"article-number":"e23193"}}