Files

1 line
38 KiB
JSON

{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,19]],"date-time":"2026-09-19T02:12:25Z","timestamp":1789783945647,"version":"4.0.1"},"reference-count":80,"publisher":"eLife Sciences Publications, Ltd","license":[{"start":{"date-parts":[[2022,10,17]],"date-time":"2022-10-17T00:00:00Z","timestamp":1665964800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2022,10,17]],"date-time":"2022-10-17T00:00:00Z","timestamp":1665964800000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2022,10,17]],"date-time":"2022-10-17T00:00:00Z","timestamp":1665964800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["EXC-2049-390688087"],"award-info":[{"award-number":["EXC-2049-390688087"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["184695641"],"award-info":[{"award-number":["184695641"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["327654276"],"award-info":[{"award-number":["327654276"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["365082554"],"award-info":[{"award-number":["365082554"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["467545627"],"award-info":[{"award-number":["467545627"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["Emmy Noether Programme"],"award-info":[{"award-number":["Emmy Noether Programme"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elifesciences.org"],"crossmark-restriction":false},"short-container-title":[],"accepted":{"date-parts":[[2022,10,17]]},"abstract":"<jats:p>\n In vertebrates, several forms of memory-relevant synaptic plasticity involve postsynaptic rearrangements of glutamate receptors. In contrast, previous work indicates that\n <jats:italic>Drosophila<\/jats:italic>\n and other invertebrates store memories using presynaptic plasticity of cholinergic synapses. Here, we provide evidence for postsynaptic plasticity at cholinergic output synapses from the\n <jats:italic>Drosophila<\/jats:italic>\n mushroom bodies (MBs). We find that the nicotinic acetylcholine receptor (nAChR) subunit \u03b15 is required within specific MB output neurons for appetitive memory induction but is dispensable for aversive memories. In addition, nAChR \u03b12 subunits mediate memory expression and likely function downstream of \u03b15 and the postsynaptic scaffold protein discs large (Dlg). We show that postsynaptic plasticity traces can be induced independently of the presynapse, and that in vivo dynamics of \u03b12 nAChR subunits are changed both in the context of associative and non-associative (familiarity) memory formation, underlying different plasticity rules. Therefore, regardless of neurotransmitter identity, key principles of postsynaptic plasticity support memory storage across phyla.\n <\/jats:p>","DOI":"10.7554\/elife.80445","type":"journal-article","created":{"date-parts":[[2022,10,17]],"date-time":"2022-10-17T08:01:57Z","timestamp":1665993717000},"update-policy":"https:\/\/doi.org\/10.7554\/elife.80445","source":"Crossref","is-referenced-by-count":32,"title":["Postsynaptic plasticity of cholinergic synapses underlies the induction and expression of appetitive and familiarity memories in Drosophila"],"prefix":"10.7554","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1893-6435","authenticated-orcid":true,"given":"Carlotta","family":"Pribbenow","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9187-930X","authenticated-orcid":true,"given":"Yi-chun","family":"Chen","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8079-4204","authenticated-orcid":true,"given":"M-Marcel","family":"Heim","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Desiree","family":"Laber","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3308-3733","authenticated-orcid":true,"given":"Silas","family":"Reubold","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8597-6173","authenticated-orcid":true,"given":"Eric","family":"Reynolds","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isabella","family":"Balles","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2462-1664","authenticated-orcid":true,"given":"Tania","family":"Fern\u00e1ndez-d V Alquicira","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5374-7963","authenticated-orcid":true,"given":"Raquel","family":"Su\u00e1rez-Grimalt","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]},{"id":[{"id":"https:\/\/ror.org\/05s5xvk70","id-type":"ROR","asserted-by":"publisher"}],"name":"Einstein Center for Neurosciences Berlin","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6013-388X","authenticated-orcid":true,"given":"Lisa","family":"Scheunemann","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]},{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"NeuroCure, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]},{"id":[{"id":"https:\/\/ror.org\/03v4gjf40","id-type":"ROR","asserted-by":"publisher"}],"name":"Institut f\u00fcr Biologie, Freie Universit\u00e4t Berlin","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carolin","family":"Rauch","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tanja","family":"Matkovic","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/03v4gjf40","id-type":"ROR","asserted-by":"publisher"}],"name":"Institut f\u00fcr Biologie, Freie Universit\u00e4t Berlin","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J\u00f6rg","family":"R\u00f6sner","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"NWFZ, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Greifswald, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5890-1958","authenticated-orcid":true,"given":"Gregor","family":"Lichtner","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]},{"id":[{"id":"https:\/\/ror.org\/025vngs54","id-type":"ROR","asserted-by":"publisher"}],"name":"Universit\u00e4tsmedizin Greifswald, Department of Anesthesia, Critical Care, Emergency and Pain Medicine","place":["Greifswald, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2078-1145","authenticated-orcid":true,"given":"Sridhar R","family":"Jagannathan","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7747-7884","authenticated-orcid":true,"given":"David","family":"Owald","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Neurophysiology, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]},{"id":[{"id":"https:\/\/ror.org\/05s5xvk70","id-type":"ROR","asserted-by":"publisher"}],"name":"Einstein Center for Neurosciences Berlin","place":["Berlin, Germany"]},{"id":[{"id":"https:\/\/ror.org\/001w7jn25","id-type":"ROR","asserted-by":"publisher"}],"name":"NeuroCure, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, corporate member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health","place":["Berlin, Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4374","published-online":{"date-parts":[[2022,10,17]]},"reference":[{"key":"bib1","doi-asserted-by":"publisher","first-page":"923","DOI":"10.15252\/embr.201540434","article-title":"Presynaptic active zones in invertebrates and vertebrates","volume":"16","author":"Ackermann","year":"2015","journal-title":"EMBO Reports"},{"key":"bib2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.04577","article-title":"The neuronal architecture of the mushroom body provides a logic for associative learning","volume":"3","author":"Aso","year":"2014","journal-title":"eLife"},{"key":"bib3","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.04580","article-title":"Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila","volume":"3","author":"Aso","year":"2014","journal-title":"eLife"},{"key":"bib4","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.16135","article-title":"Dopaminergic neurons write and update memories with cell-type-specific rules","volume":"5","author":"Aso","year":"2016","journal-title":"eLife"},{"key":"bib5","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.49257","article-title":"Nitric oxide acts as a cotransmitter in a subset of dopaminergic neurons to diversify memory dynamics","volume":"8","author":"Aso","year":"2019","journal-title":"eLife"},{"key":"bib6","doi-asserted-by":"publisher","first-page":"1899","DOI":"10.1242\/jcs.01029","article-title":"Cell type-specific recruitment of Drosophila lin-7 to distinct MAGUK-based protein complexes defines novel roles for sdt and dlg-S97","volume":"117","author":"Bachmann","year":"2004","journal-title":"Journal of Cell Science"},{"key":"bib7","doi-asserted-by":"publisher","first-page":"1237","DOI":"10.1016\/j.neuron.2016.02.015","article-title":"Memory-relevant mushroom body output synapses are cholinergic","volume":"89","author":"Barnstedt","year":"2016","journal-title":"Neuron"},{"key":"bib8","article-title":"Neuprint-python","volume-title":"GitHub","author":"Berg","year":"2022","unstructured":"Berg S, Schlegel P, Svirskas R. 2022. Neuprint-python. GitHub. https:\/\/github.com\/connectome-neuprint\/neuprint-python."},{"key":"bib9","doi-asserted-by":"publisher","first-page":"963","DOI":"10.1016\/j.neuron.2020.03.010","article-title":"Visualization of a distributed synaptic memory code in the Drosophila brain","volume":"106","author":"Bilz","year":"2020","journal-title":"Neuron"},{"key":"bib10","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1113\/jphysiol.1973.sp010273","article-title":"Long-Lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path","volume":"232","author":"Bliss","year":"1973","journal-title":"The Journal of Physiology"},{"key":"bib11","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-08977-6","article-title":"Rapid active zone remodeling consolidates presynaptic potentiation","volume":"10","author":"B\u00f6hme","year":"2019","journal-title":"Nature Communications"},{"key":"bib12","doi-asserted-by":"publisher","first-page":"822","DOI":"10.1016\/j.cub.2014.03.021","article-title":"Dopaminergic modulation of cAMP drives nonlinear plasticity across the Drosophila mushroom body lobes","volume":"24","author":"Boto","year":"2014","journal-title":"Current Biology"},{"key":"bib13","doi-asserted-by":"publisher","first-page":"1280","DOI":"10.1016\/j.celrep.2015.04.044","article-title":"Two independent mushroom body output circuits retrieve the six discrete components of Drosophila aversive memory","volume":"11","author":"Bouzaiane","year":"2015","journal-title":"Cell Reports"},{"key":"bib14","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.23789","article-title":"Reciprocal synapses between mushroom body and dopamine neurons form a positive feedback loop required for learning","volume":"6","author":"Cervantes-Sandoval","year":"2017","journal-title":"eLife"},{"key":"bib15","doi-asserted-by":"publisher","DOI":"10.1101\/2020.01.16.909465","article-title":"neuPrint: Analysis Tools for EM Connectomics","volume-title":"bioRxiv","author":"Clements","year":"2020"},{"key":"bib16","doi-asserted-by":"publisher","first-page":"1742","DOI":"10.1016\/j.cell.2015.11.019","article-title":"Coordinated and compartmentalized neuromodulation shapes sensory processing in Drosophila","volume":"163","author":"Cohn","year":"2015","journal-title":"Cell"},{"key":"bib17","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1101\/lm.5.1.38","article-title":"Tripartite mushroom body architecture revealed by antigenic markers","volume":"5","author":"Crittenden","year":"1998","journal-title":"Learning & Memory"},{"key":"bib18","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1007\/978-1-4419-6445-8_2","article-title":"The evolution of pentameric ligand-gated ion channels","volume":"683","author":"Dent","year":"2010","journal-title":"Advances in Experimental Medicine and Biology"},{"key":"bib19","doi-asserted-by":"publisher","first-page":"476","DOI":"10.1038\/35078077","article-title":"Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory","volume":"411","author":"Dubnau","year":"2001","journal-title":"Nature"},{"key":"bib20","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2020.108119","article-title":"Cholinergic synaptic homeostasis is tuned by an NFAT-mediated \u03b17 nachr-kv4\/shal coupled regulatory system","volume":"32","author":"Eadaim","year":"2020","journal-title":"Cell Reports"},{"key":"bib21","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1016\/j.neures.2017.11.015","article-title":"Drosophila active zones: from molecules to behaviour","volume":"127","author":"Ehmann","year":"2018","journal-title":"Neuroscience Research"},{"key":"bib22","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1038\/nature23455","article-title":"The complete connectome of a learning and memory centre in an insect brain","volume":"548","author":"Eichler","year":"2017","journal-title":"Nature"},{"key":"bib23","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1038\/nature21716","article-title":"Re-Evaluation of learned information in Drosophila","volume":"544","author":"Felsenberg","year":"2017","journal-title":"Nature"},{"key":"bib24","doi-asserted-by":"publisher","first-page":"709","DOI":"10.1016\/j.cell.2018.08.021","article-title":"Integration of parallel opposing memories underlies memory extinction","volume":"175","author":"Felsenberg","year":"2018","journal-title":"Cell"},{"key":"bib25","doi-asserted-by":"publisher","first-page":"R31","DOI":"10.1016\/j.cub.2009.10.023","article-title":"Common mechanisms of synaptic plasticity in vertebrates and invertebrates","volume":"20","author":"Glanzman","year":"2010","journal-title":"Current Biology"},{"key":"bib26","doi-asserted-by":"publisher","first-page":"807","DOI":"10.1016\/s0896-6273(03)00714-1","article-title":"Calcium microdomains in aspiny dendrites","volume":"40","author":"Goldberg","year":"2003","journal-title":"Neuron"},{"key":"bib27","doi-asserted-by":"publisher","first-page":"713","DOI":"10.1016\/j.neuron.2017.04.009","article-title":"Structural and functional architecture of AMPA-type glutamate receptors and their auxiliary proteins","volume":"94","author":"Greger","year":"2017","journal-title":"Neuron"},{"key":"bib28","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1016\/S0006-3495(70)86308-1","article-title":"Dark current and photocurrent in retinal rods","volume":"10","author":"Hagins","year":"1970","journal-title":"Biophysical Journal"},{"key":"bib29","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-022-14413-5","article-title":"Visualization of Learning-induced synaptic plasticity in output neurons of the Drosophila mushroom body \u03b3-lobe","volume":"12","author":"Hancock","year":"2022","journal-title":"Scientific Reports"},{"key":"bib30","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1016\/j.cell.2019.05.040","article-title":"Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning","volume":"178","author":"Handler","year":"2019","journal-title":"Cell"},{"key":"bib31","doi-asserted-by":"publisher","first-page":"956","DOI":"10.1016\/j.cell.2017.04.028","article-title":"Representations of novelty and familiarity in a mushroom body compartment","volume":"169","author":"Hattori","year":"2017","journal-title":"Cell"},{"key":"bib32","doi-asserted-by":"publisher","first-page":"985","DOI":"10.1016\/j.neuron.2015.11.003","article-title":"Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila","volume":"88","author":"Hige","year":"2015","journal-title":"Neuron"},{"key":"bib33","doi-asserted-by":"publisher","first-page":"11772","DOI":"10.1523\/JNEUROSCI.1099-11.2011","article-title":"Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body","volume":"31","author":"Honegger","year":"2011","journal-title":"The Journal of Neuroscience"},{"key":"bib34","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.10719","article-title":"Reward signal in a recurrent circuit drives appetitive long-term memory formation","volume":"4","author":"Ichinose","year":"2015","journal-title":"eLife"},{"key":"bib35","doi-asserted-by":"publisher","first-page":"1294","DOI":"10.1016\/j.cub.2020.12.032","article-title":"Mushroom body output differentiates memory processes and distinct memory-guided behaviors","volume":"31","author":"Ichinose","year":"2021","journal-title":"Current Biology"},{"key":"bib36","doi-asserted-by":"publisher","first-page":"16283","DOI":"10.1073\/pnas.2003667117","article-title":"Cofactor-enabled functional expression of fruit fly, honeybee, and bumblebee nicotinic receptors reveals picomolar neonicotinoid actions","volume":"117","author":"Ihara","year":"2020","journal-title":"PNAS"},{"key":"bib37","doi-asserted-by":"publisher","first-page":"1143","DOI":"10.1152\/physrev.2001.81.3.1143","article-title":"Cerebellar long-term depression: characterization, signal transduction, and functional roles","volume":"81","author":"Ito","year":"2001","journal-title":"Physiological Reviews"},{"key":"bib38","article-title":"Postsynapticplasticity","volume-title":"Software Heritage","author":"Jagannathan","year":"2022","unstructured":"Jagannathan S. 2022. Postsynapticplasticity. Software Heritage. swh:1:rev:0550ee981ec5b6eb7e76e9062e3c9c8dead42306. https:\/\/archive.softwareheritage.org\/swh:1:dir:6e3eb90d9f713e67ab67fd52ac62d455dc7e803b;origin=https:\/\/github.com\/owaldlab\/2022_postsynapticplasticity;visit=swh:1:snp:704e43b1d1e66683eba9496f91aec488c4399d98;anchor=swh:1:rev:0550ee981ec5b6eb7e76e9062e3c9c8dead42306."},{"key":"bib39","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1016\/j.cell.2014.03.001","article-title":"The molecular and systems biology of memory","volume":"157","author":"Kandel","year":"2014","journal-title":"Cell"},{"key":"bib40","doi-asserted-by":"publisher","first-page":"7640","DOI":"10.1523\/JNEUROSCI.1167-07.2007","article-title":"D1 dopamine receptor dda1 is required in the mushroom body neurons for aversive and appetitive learning in Drosophila","volume":"27","author":"Kim","year":"2007","journal-title":"The Journal of Neuroscience"},{"key":"bib41","doi-asserted-by":"publisher","first-page":"715","DOI":"10.1534\/genetics.113.156737","article-title":"Highly improved gene targeting by germline-specific Cas9 expression in Drosophila","volume":"195","author":"Kondo","year":"2013","journal-title":"Genetics"},{"key":"bib42","doi-asserted-by":"publisher","first-page":"647","DOI":"10.1152\/physrev.00010.2015","article-title":"Cellular and system biology of memory: timing, molecules, and beyond","volume":"96","author":"Korte","year":"2016","journal-title":"Physiological Reviews"},{"key":"bib43","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1016\/j.neuron.2006.11.021","article-title":"Sequential use of mushroom body neuron subsets during Drosophila odor memory processing","volume":"53","author":"Krashes","year":"2007","journal-title":"Neuron"},{"key":"bib44","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2202-13-73","article-title":"The Drosophila nicotinic acetylcholine receptor subunits D\u03b15 and D\u03b17 form functional homomeric and heteromeric ion channels","volume":"13","author":"Lansdell","year":"2012","journal-title":"BMC Neuroscience"},{"key":"bib45","doi-asserted-by":"publisher","first-page":"2203","DOI":"10.1016\/j.cub.2015.07.015","article-title":"A higher brain circuit for immediate integration of conflicting sensory information in Drosophila","volume":"25","author":"Lewis","year":"2015","journal-title":"Current Biology"},{"key":"bib46","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1038\/nn.3660","article-title":"Sparse, decorrelated odor coding in the mushroom body enhances learned odor discrimination","volume":"17","author":"Lin","year":"2014","journal-title":"Nature Neuroscience"},{"key":"bib47","doi-asserted-by":"publisher","first-page":"1536","DOI":"10.1038\/nn.3827","article-title":"Neural correlates of water reward in thirsty Drosophila","volume":"17","author":"Lin","year":"2014","journal-title":"Nature Neuroscience"},{"key":"bib48","doi-asserted-by":"publisher","first-page":"650","DOI":"10.1016\/j.neuron.2011.01.017","article-title":"Drug-Evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling","volume":"69","author":"L\u00fcscher","year":"2011","journal-title":"Neuron"},{"key":"bib49","doi-asserted-by":"publisher","first-page":"1330","DOI":"10.1126\/science.1062622","article-title":"The role of Drosophila mushroom body signaling in olfactory memory","volume":"293","author":"McGuire","year":"2001","journal-title":"Science"},{"key":"bib50","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1016\/j.neuron.2016.12.015","article-title":"A brief history of long-term potentiation","volume":"93","author":"Nicoll","year":"2017","journal-title":"Neuron"},{"key":"bib51","doi-asserted-by":"publisher","DOI":"10.3389\/fnins.2020.00712","article-title":"NOSA, an analytical toolbox for multicellular optical electrophysiology","volume":"14","author":"Oltmanns","year":"2020","journal-title":"Frontiers in Neuroscience"},{"key":"bib52","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1016\/j.conb.2009.03.003","article-title":"Assembling the presynaptic active zone","volume":"19","author":"Owald","year":"2009","journal-title":"Current Opinion in Neurobiology"},{"key":"bib53","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1016\/j.neuron.2015.03.025","article-title":"Activity of defined mushroom body output neurons underlies learned olfactory behavior in Drosophila","volume":"86","author":"Owald","year":"2015","journal-title":"Neuron"},{"key":"bib54","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1016\/j.conb.2015.10.002","article-title":"Olfactory learning skews mushroom body output pathways to steer behavioral choice in Drosophila","volume":"35","author":"Owald","year":"2015","journal-title":"Current Opinion in Neurobiology"},{"key":"bib55","doi-asserted-by":"publisher","first-page":"7898","DOI":"10.1073\/pnas.1216336110","article-title":"Drosophila orb protein in two mushroom body output neurons is necessary for long-term memory formation","volume":"110","author":"Pai","year":"2013","journal-title":"PNAS"},{"key":"bib56","doi-asserted-by":"publisher","first-page":"945","DOI":"10.1016\/j.neuron.2013.07.045","article-title":"Different kenyon cell populations drive learned approach and avoidance in Drosophila","volume":"79","author":"Perisse","year":"2013","journal-title":"Neuron"},{"key":"bib57","doi-asserted-by":"publisher","first-page":"1086","DOI":"10.1016\/j.neuron.2016.04.034","article-title":"Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body","volume":"90","author":"Perisse","year":"2016","journal-title":"Neuron"},{"key":"bib58","doi-asserted-by":"publisher","first-page":"769","DOI":"10.1016\/j.celrep.2013.09.032","article-title":"Two pairs of mushroom body efferent neurons are required for appetitive long-term memory retrieval in Drosophila","volume":"5","author":"Pla\u00e7ais","year":"2013","journal-title":"Cell Reports"},{"key":"bib59","doi-asserted-by":"publisher","first-page":"608","DOI":"10.1016\/j.cub.2012.02.014","article-title":"Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila","volume":"22","author":"Qin","year":"2012","journal-title":"Current Biology"},{"key":"bib60","doi-asserted-by":"publisher","first-page":"3611","DOI":"10.1016\/j.cub.2019.08.070","article-title":"Network-specific synchronization of electrical slow-wave oscillations regulates sleep drive in Drosophila","volume":"29","author":"Raccuglia","year":"2019","journal-title":"Current Biology"},{"key":"bib61","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1080\/01677060802471684","article-title":"Synaptic organization of lobula plate tangential cells in Drosophila: Dalpha7 cholinergic receptors","volume":"23","author":"Raghu","year":"2009","journal-title":"Journal of Neurogenetics"},{"key":"bib62","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.57443","article-title":"A connectome and analysis of the adult Drosophila central brain","volume":"9","author":"Scheffer","year":"2020","journal-title":"eLife"},{"key":"bib63","doi-asserted-by":"publisher","first-page":"951","DOI":"10.1016\/s0896-6273(02)00832-2","article-title":"Extinction antagonizes olfactory memory at the subcellular level","volume":"35","author":"Schwaerzel","year":"2002","journal-title":"Neuron"},{"key":"bib64","doi-asserted-by":"publisher","first-page":"903","DOI":"10.1038\/nn.2846","article-title":"Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila","volume":"14","author":"S\u00e9journ\u00e9","year":"2011","journal-title":"Nature Neuroscience"},{"key":"bib65","doi-asserted-by":"publisher","first-page":"1773","DOI":"10.1016\/j.cub.2011.09.011","article-title":"Alternative sites of synaptic plasticity in two homologous \u201c fan-out fan-in \u201d learning and memory networks","volume":"21","author":"Shomrat","year":"2011","journal-title":"Current Biology"},{"key":"bib66","doi-asserted-by":"publisher","first-page":"1349","DOI":"10.1016\/j.cub.2013.05.060","article-title":"DLin-7 is required in postsynaptic lamina neurons to prevent light-induced photoreceptor degeneration in Drosophila","volume":"23","author":"Soukup","year":"2013","journal-title":"Current Biology"},{"key":"bib67","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.76712","article-title":"Associative learning drives longitudinally graded presynaptic plasticity of neurotransmitter release along axonal compartments","volume":"11","author":"Stahl","year":"2022","journal-title":"eLife"},{"key":"bib68","doi-asserted-by":"publisher","first-page":"1713","DOI":"10.1038\/nn.4157","article-title":"Dendritic integration: 60 years of progress","volume":"18","author":"Stuart","year":"2015","journal-title":"Nature Neuroscience"},{"key":"bib69","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.26975","article-title":"A connectome of A learning and memory center in the adult Drosophila brain","volume":"6","author":"Takemura","year":"2017","journal-title":"eLife"},{"key":"bib70","doi-asserted-by":"publisher","first-page":"210","DOI":"10.1038\/nature19058","article-title":"A trans-synaptic nanocolumn aligns neurotransmitter release to receptors","volume":"536","author":"Tang","year":"2016","journal-title":"Nature"},{"key":"bib71","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1017\/S0033583510000168","article-title":"The structural basis of function in Cys-loop receptors","volume":"43","author":"Thompson","year":"2010","journal-title":"Quarterly Reviews of Biophysics"},{"key":"bib72","doi-asserted-by":"publisher","first-page":"1647","DOI":"10.1016\/j.cub.2011.08.032","article-title":"Parallel processing of appetitive short- and long-term memories in Drosophila","volume":"21","author":"Trannoy","year":"2011","journal-title":"Current Biology"},{"key":"bib73","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/0092-8674(94)90398-0","article-title":"Genetic dissection of consolidated memory in Drosophila","volume":"79","author":"Tully","year":"1994","journal-title":"Cell"},{"key":"bib74","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.21076","article-title":"Coincident postsynaptic activity gates presynaptic dopamine release to induce plasticity in Drosophila mushroom bodies","volume":"6","author":"Ueno","year":"2017","journal-title":"eLife"},{"key":"bib75","doi-asserted-by":"publisher","first-page":"3533","DOI":"10.1523\/JNEUROSCI.2378-19.2020","article-title":"Carbon monoxide, a retrograde messenger generated in postsynaptic mushroom body neurons, evokes noncanonical dopamine release","volume":"40","author":"Ueno","year":"2020","journal-title":"The Journal of Neuroscience"},{"key":"bib76","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.39196","article-title":"Multiple neurons encode crebb dependent appetitive long-term memory in the mushroom body circuit","volume":"7","author":"Widmer","year":"2018","journal-title":"eLife"},{"key":"bib77","doi-asserted-by":"publisher","first-page":"94","DOI":"10.1016\/j.conb.2017.01.006","article-title":"Maguks: multifaceted synaptic organizers","volume":"43","author":"Won","year":"2017","journal-title":"Current Opinion in Neurobiology"},{"key":"bib78","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-017-07600-2","article-title":"Long-Term memory requires sequential protein synthesis in three subsets of mushroom body output neurons in Drosophila","volume":"7","author":"Wu","year":"2017","journal-title":"Scientific Reports"},{"key":"bib79","doi-asserted-by":"publisher","first-page":"2346","DOI":"10.1016\/j.celrep.2018.02.012","article-title":"Two parallel pathways assign opposing odor valences during Drosophila memory formation","volume":"22","author":"Yamazaki","year":"2018","journal-title":"Cell Reports"},{"key":"bib80","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.31425","article-title":"Persistent activity in a recurrent circuit underlies courtship memory in Drosophila","volume":"7","author":"Zhao","year":"2018","journal-title":"eLife"}],"container-title":["eLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/cdn.elifesciences.org\/articles\/80445\/elife-80445-v2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/cdn.elifesciences.org\/articles\/80445\/elife-80445-v2.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/elifesciences.org\/articles\/80445","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,11]],"date-time":"2023-10-11T21:24:01Z","timestamp":1697059441000},"score":1,"resource":{"primary":{"URL":"https:\/\/elifesciences.org\/articles\/80445"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,17]]},"references-count":80,"alternative-id":["10.7554\/eLife.80445"],"URL":"https:\/\/doi.org\/10.7554\/elife.80445","archive":["CLOCKSS"],"relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2022.07.15.500172","asserted-by":"subject"}],"has-review":[{"id-type":"doi","id":"10.7554\/eLife.80445.sa2","asserted-by":"object"},{"id-type":"doi","id":"10.7554\/eLife.80445.sa0","asserted-by":"object"},{"id-type":"doi","id":"10.7554\/eLife.80445.sa1","asserted-by":"object"}]},"ISSN":["2050-084X"],"issn-type":[{"value":"2050-084X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,17]]},"assertion":[{"value":"single anonymised","name":"peer_review_transparency","label":"Peer review transparency","group":{"name":"peer_review_taxonomy"}},{"value":"other reviewer(s), editor","name":"peer_review_interaction","label":"Peer review interaction","group":{"name":"peer_review_taxonomy"}},{"value":"review summaries, review reports, author\/editor communication, reviewer identities reviewer opt in, editor identities","name":"peer_review_published","label":"Peer review published","group":{"name":"peer_review_taxonomy"}},{"value":"open (sign in with ORCID iD required)","name":"post_publication_commenting","label":"Post publication commenting","group":{"name":"post_publication_commenting"}}],"article-number":"e80445"}}