{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,26]],"date-time":"2026-02-26T15:12:06Z","timestamp":1772118726558,"version":"3.50.1"},"reference-count":78,"publisher":"Wiley","issue":"10","license":[{"start":{"date-parts":[[2024,10,7]],"date-time":"2024-10-07T00:00:00Z","timestamp":1728259200000},"content-version":"vor","delay-in-days":6,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"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"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["J of Neuroscience Research"],"published-print":{"date-parts":[[2024,10]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Visceral feedback from the body is often subconscious, but plays an important role in guiding motivated behaviors. Vagal sensory neurons relay \u201cgut feelings\u201d to noradrenergic (NA) neurons in the caudal nucleus of the solitary tract (cNTS), which in turn project to the anterior ventrolateral bed nucleus of the stria terminalis (vlBNST) and other hypothalamic\u2010limbic forebrain regions. Prior work supports a role for these circuits in modulating memory consolidation and extinction, but a potential role in retrieval of conditioned avoidance remains untested. To examine this, adult male rats underwent passive avoidance conditioning. We then lesioned gut\u2010sensing vagal afferents by injecting cholecystokinin\u2010conjugated saporin toxin (CSAP) into the vagal nodose ganglia (Experiment 1), or lesioned NA inputs to the vlBNST by injecting saporin toxin conjugated to an antibody against dopamine\u2010beta hydroxylase (DSAP) into the vlBNST (Experiment 2). When avoidance behavior was later assessed, rats with vagal CSAP lesions or NA DSAP lesions displayed significantly increased conditioned passive avoidance. These new findings support the view that gut vagal afferents and the cNTS\n                    <jats:sup>NA<\/jats:sup>\n                    \u2010to\u2010vlBNST circuit play a role in modulating the expression\/retrieval of learned passive avoidance. Overall, our data suggest a dynamic modulatory role of vagal sensory feedback to the limbic forebrain in integrating interoceptive signals with contextual cues that elicit conditioned avoidance behavior.\n                  <\/jats:p>","DOI":"10.1002\/jnr.25390","type":"journal-article","created":{"date-parts":[[2024,10,7]],"date-time":"2024-10-07T08:44:01Z","timestamp":1728290641000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Ascending Vagal Sensory and Central Noradrenergic Pathways Modulate Retrieval of Passive Avoidance Memory in Male Rats"],"prefix":"10.1002","volume":"102","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3692-7495","authenticated-orcid":false,"given":"Caitlyn\u00a0M.","family":"Edwards","sequence":"first","affiliation":[{"name":"Department of Psychology, Program in Neuroscience Florida State University  Tallahassee Florida USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Inge\u00a0Estefania","family":"Guerrero","sequence":"additional","affiliation":[{"name":"Department of Psychology, Program in Neuroscience Florida State University  Tallahassee Florida USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Danielle","family":"Thompson","sequence":"additional","affiliation":[{"name":"Department of Psychology, Program in Neuroscience Florida State University  Tallahassee Florida USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tyla","family":"Dolezel","sequence":"additional","affiliation":[{"name":"Department of Psychology, Program in Neuroscience Florida State University  Tallahassee Florida USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Linda","family":"Rinaman","sequence":"additional","affiliation":[{"name":"Department of Psychology, Program in Neuroscience Florida State University  Tallahassee Florida USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"311","published-online":{"date-parts":[[2024,10,7]]},"reference":[{"key":"e_1_2_13_2_1","doi-asserted-by":"publisher","DOI":"10.1155\/2016\/4273280"},{"key":"e_1_2_13_3_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3502-07.2007"},{"key":"e_1_2_13_4_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0163-1047(85)91580-8"},{"key":"e_1_2_13_5_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1749-6632.1999.tb09284.x"},{"key":"e_1_2_13_6_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3561-06.2006"},{"key":"e_1_2_13_7_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF02244229"},{"key":"e_1_2_13_8_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1460-9568.2003.02967.x"},{"key":"e_1_2_13_9_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2008.08.011"},{"key":"e_1_2_13_10_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00429-012-0393-6"},{"key":"e_1_2_13_11_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fpsyt.2018.00044","article-title":"Vagus Nerve as Modulator of the Brain\u2010Gut Axis in Psychiatric and Inflammatory Disorders","volume":"9","author":"Breit S.","year":"2018","journal-title":"Frontiers in Psychiatry"},{"key":"e_1_2_13_12_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fnins.2021.782786","article-title":"Self\u2010Administration of Right Vagus Nerve Stimulation Activates Midbrain Dopaminergic Nuclei","volume":"15","author":"Brougher J.","year":"2021","journal-title":"Frontiers in Neuroscience"},{"key":"e_1_2_13_13_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1523\/ENEURO.0205-19.2019","article-title":"Estimation for Better Inference in Neuroscience","volume":"6","author":"Calin\u2010Jageman R.","year":"2019","journal-title":"eNeuro"},{"key":"e_1_2_13_14_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2020.07.084"},{"key":"e_1_2_13_15_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tins.2020.10.007"},{"key":"e_1_2_13_16_1","doi-asserted-by":"publisher","DOI":"10.1006\/nlme.1995.1024"},{"key":"e_1_2_13_17_1","doi-asserted-by":"publisher","DOI":"10.1038\/4600"},{"key":"e_1_2_13_18_1","doi-asserted-by":"publisher","DOI":"10.1006\/nlme.1998.3863"},{"key":"e_1_2_13_19_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.0953-816x.2001.01733.x"},{"key":"e_1_2_13_20_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0006-8993(98)00672-6"},{"key":"e_1_2_13_21_1","doi-asserted-by":"publisher","DOI":"10.1152\/ajpgi.00095.2017"},{"key":"e_1_2_13_22_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.physbeh.2021.113511"},{"key":"e_1_2_13_23_1","volume-title":"Visceral Feedback Modulation of Conditioned Avoidance Behavior","author":"Edwards C","year":"2022"},{"key":"e_1_2_13_24_1","doi-asserted-by":"publisher","DOI":"10.1159\/000528828"},{"key":"e_1_2_13_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainresrev.2004.07.011"},{"key":"e_1_2_13_26_1","doi-asserted-by":"publisher","DOI":"10.1021\/acschemneuro.6b00210"},{"key":"e_1_2_13_27_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.brs.2008.02.001"},{"issue":"3","key":"e_1_2_13_28_1","first-page":"84","article-title":"The Influence of Vagus Nerve Stimulation on Memory","volume":"50","author":"Ghacibeh G. A.","year":"2009","journal-title":"Epilepsia"},{"key":"e_1_2_13_29_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00213\u2010023\u201006453\u20100"},{"key":"e_1_2_13_30_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neubiorev.2005.01.004"},{"key":"e_1_2_13_31_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41386-023-01581-9"},{"key":"e_1_2_13_32_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2018.08.049"},{"key":"e_1_2_13_33_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0920-1211(01)00291-1"},{"key":"e_1_2_13_34_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41592\u2010019\u20100470\u20103"},{"key":"e_1_2_13_35_1","doi-asserted-by":"publisher","DOI":"10.1016\/0014-5793(92)80042-F"},{"key":"e_1_2_13_36_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.0252\u201014.2014"},{"key":"e_1_2_13_37_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.biopsych.2022.04.020"},{"key":"e_1_2_13_38_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fnbeh.2015.00189","article-title":"Avoidance Learning: A Review of Theoretical Models and Recent Developments","volume":"9","author":"Krypotos A. M.","year":"2015","journal-title":"Frontiers in Behavioral Neuroscience"},{"key":"e_1_2_13_39_1","first-page":"724","article-title":"Effects of DSP\u20104\u2010Induced Depletion of Brain Norepinephrine on Appetitive and Aversive Memory Retrieval","volume":"32","author":"Kumar K. B.","year":"1994","journal-title":"Indian Journal of Experimental Biology"},{"key":"e_1_2_13_40_1","first-page":"1","article-title":"Non\u2010invasive Vagal Nerve Stimulation Effects on Hyperarousal and Autonomic State in Patients With Posttraumatic Stress Disorder and History of Mild Traumatic Brain Injury: Preliminary Evidence","volume":"4","author":"Lamb D. G.","year":"2017","journal-title":"Frontiers in Medicine"},{"key":"e_1_2_13_41_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467\u2010021\u201023674\u2010z"},{"key":"e_1_2_13_42_1","doi-asserted-by":"publisher","DOI":"10.1152\/physiol.00036.2017"},{"key":"e_1_2_13_43_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3464\u201014.2015"},{"key":"e_1_2_13_44_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrn3071"},{"key":"e_1_2_13_45_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cmet.2023.12.014"},{"key":"e_1_2_13_46_1","doi-asserted-by":"publisher","DOI":"10.1111\/apha.13530"},{"key":"e_1_2_13_47_1","doi-asserted-by":"publisher","DOI":"10.1002\/dev.21187"},{"key":"e_1_2_13_48_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0031-9384(02)00925-3"},{"key":"e_1_2_13_49_1","doi-asserted-by":"publisher","DOI":"10.1038\/tp.2017.191"},{"key":"e_1_2_13_50_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fnins.2019.00911","article-title":"Vagus Nerve Stimulation in Rodent Models: An Overview of Technical Considerations","volume":"13","author":"Noller C. M.","year":"2019","journal-title":"Frontiers in Neuroscience"},{"key":"e_1_2_13_51_1","doi-asserted-by":"publisher","DOI":"10.4103\/0976-9668.107254"},{"key":"e_1_2_13_52_1","doi-asserted-by":"publisher","DOI":"10.1002\/ar.10026"},{"key":"e_1_2_13_53_1","doi-asserted-by":"publisher","DOI":"10.3389\/fnbeh.2014.00327\/abstract"},{"key":"e_1_2_13_54_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.biopsych.2012.10.021"},{"key":"e_1_2_13_55_1","doi-asserted-by":"publisher","DOI":"10.1016\/0361-9230(92)90218-M"},{"key":"e_1_2_13_56_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.nlm.2010.07.002"},{"key":"e_1_2_13_57_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-022-05139-5"},{"key":"e_1_2_13_58_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2008.04.007"},{"key":"e_1_2_13_59_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902930306"},{"key":"e_1_2_13_60_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.23-31-10084.2003"},{"key":"e_1_2_13_61_1","doi-asserted-by":"publisher","DOI":"10.1152\/ajpregu.00556.2010"},{"key":"e_1_2_13_62_1","doi-asserted-by":"publisher","DOI":"10.1152\/ajpregu.00393.2007"},{"key":"e_1_2_13_63_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.10-02-00531.1990"},{"key":"e_1_2_13_64_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902380411"},{"key":"e_1_2_13_65_1","doi-asserted-by":"publisher","DOI":"10.1037\/h0035967"},{"key":"e_1_2_13_66_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467\u2010018\u201004639\u20101"},{"key":"e_1_2_13_67_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2004.06.015"},{"key":"e_1_2_13_68_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-020-58412-w"},{"key":"e_1_2_13_69_1","doi-asserted-by":"publisher","DOI":"10.1016\/0006-8993(94)01453-O"},{"key":"e_1_2_13_70_1","doi-asserted-by":"publisher","DOI":"10.1037\/0735-7044.111.3.579"},{"key":"e_1_2_13_71_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neubiorev.2014.05.005"},{"key":"e_1_2_13_72_1","doi-asserted-by":"publisher","DOI":"10.1037\/0735-7044.120.2.324"},{"key":"e_1_2_13_73_1","doi-asserted-by":"publisher","DOI":"10.1038\/nprot.2007.44"},{"key":"e_1_2_13_74_1","doi-asserted-by":"publisher","DOI":"10.1016\/0196-9781(86)90076-8"},{"key":"e_1_2_13_75_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.brs.2020.07.002"},{"key":"e_1_2_13_76_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0006-8993(96)00855-4"},{"key":"e_1_2_13_77_1","doi-asserted-by":"publisher","DOI":"10.1111\/ejn.12123"},{"key":"e_1_2_13_78_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1460-9568.2002.02285.x"},{"key":"e_1_2_13_79_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.nlm.2010.11.002"}],"container-title":["Journal of Neuroscience Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/jnr.25390","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,25]],"date-time":"2024-10-25T06:19:33Z","timestamp":1729837173000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/jnr.25390"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10]]},"references-count":78,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2024,10]]}},"alternative-id":["10.1002\/jnr.25390"],"URL":"https:\/\/doi.org\/10.1002\/jnr.25390","archive":["Portico"],"relation":{"has-review":[{"id-type":"doi","id":"10.1002\/JNR.25390\/v2\/review2","asserted-by":"object"},{"id-type":"doi","id":"10.1002\/JNR.25390\/v2\/decision1","asserted-by":"object"},{"id-type":"doi","id":"10.1002\/JNR.25390\/v2\/response1","asserted-by":"object"},{"id-type":"doi","id":"10.1002\/JNR.25390\/v1\/review3","asserted-by":"object"},{"id-type":"doi","id":"10.1002\/JNR.25390\/v1\/review2","asserted-by":"object"},{"id-type":"doi","id":"10.1002\/JNR.25390\/v1\/review1","asserted-by":"object"},{"id-type":"doi","id":"10.1002\/JNR.25390\/v2\/review1","asserted-by":"object"},{"id-type":"doi","id":"10.1002\/JNR.25390\/v1\/decision1","asserted-by":"object"}]},"ISSN":["0360-4012","1097-4547"],"issn-type":[{"value":"0360-4012","type":"print"},{"value":"1097-4547","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10]]},"assertion":[{"value":"2024-04-26","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-09-18","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-10-07","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e25390"}}