{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,4]],"date-time":"2026-05-04T20:31:48Z","timestamp":1777926708654,"version":"3.51.4"},"reference-count":88,"publisher":"SAGE Publications","issue":"14","license":[{"start":{"date-parts":[[2014,7,1]],"date-time":"2014-07-01T00:00:00Z","timestamp":1404172800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.sagepub.com\/page\/policies\/text-and-data-mining-license"}],"content-domain":{"domain":["journals.sagepub.com"],"crossmark-restriction":true},"short-container-title":["Journal of Neurotrauma"],"published-print":{"date-parts":[[2014,7]]},"abstract":"<jats:p>\n                    Loss of olfactory function is an early indicator of traumatic brain injury (TBI). The regenerative capacity and well-defined neural maps of the mammalian olfactory system enable investigations into the degeneration and recovery of neural circuits after injury. Here, we introduce a unique olfactory-based model of TBI that reproduces many hallmarks associated with human brain trauma. We performed a unilateral penetrating impact to the mouse olfactory bulb and observed a significant loss of olfactory sensory neurons (OSNs) in the olfactory epithelium (OE) ipsilateral to the injury, but not contralateral. By comparison, we detected the injury markers p75\n                    <jats:sup>NTR<\/jats:sup>\n                    , \u03b2-APP, and activated caspase-3 in both the ipsi- and contralateral OE. In the olfactory bulb (OB), we observed a graded cell loss, with ipsilateral showing a greater reduction than contralateral and both significantly less than sham. Similar to OE, injury markers in the OB were primarily detected on the ipsilateral side, but also observed contralaterally. Behavioral experiments measured 4 days after impact also demonstrated loss of olfactory function, yet following a 30-day recovery period, we observed a significant improvement in olfactory function and partial recovery of olfactory circuitry, despite the persistence of TBI markers. Interestingly, by using the M71-IRES-tauLacZ reporter line to track OSN organization, we further determined that inducing neural activity during the recovery period with intense odor conditioning did not enhance the recovery process. Together, these data establish the mouse olfactory system as a new model to study TBI, serving as a platform to understand neural disruption and the potential for circuit restoration.\n                  <\/jats:p>","DOI":"10.1089\/neu.2013.3296","type":"journal-article","created":{"date-parts":[[2014,4,3]],"date-time":"2014-04-03T01:43:17Z","timestamp":1396489397000},"page":"1277-1291","update-policy":"https:\/\/doi.org\/10.1177\/sage-journals-update-policy","source":"Crossref","is-referenced-by-count":12,"title":["Using the Olfactory System as an\n                    <i>In Vivo<\/i>\n                    Model To Study Traumatic Brain Injury and Repair"],"prefix":"10.1177","volume":"31","author":[{"given":"Elizabeth","family":"Steuer","sequence":"first","affiliation":[{"name":"National Institutes of Health"},{"name":"Uniformed Services University"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michele L.","family":"Schaefer","sequence":"additional","affiliation":[{"name":"National Institutes of Health"},{"name":"Uniformed Services University"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Leonardo","family":"Belluscio","sequence":"additional","affiliation":[{"name":"National Institutes of Health"},{"name":"Uniformed Services University"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"179","published-online":{"date-parts":[[2014,7,15]]},"reference":[{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1136\/ip.2010.029215.951"},{"key":"e_1_3_3_3_2","doi-asserted-by":"crossref","unstructured":"Finkelstein E. Corso P.S. and Miller T.R. (2006). The incidence and economic burden of injuries in the United States. Oxford University Press: Oxford UK.","DOI":"10.1093\/acprof:oso\/9780195179484.001.0001"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1097\/01.WCB.0000111614.19196.04"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.2174\/1381612043384060"},{"key":"e_1_3_3_6_2","doi-asserted-by":"publisher","DOI":"10.1093\/brain\/87.1.107"},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1097\/00001199-200206000-00006"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1001\/archneur.1997.00550210061014"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.otc.2004.06.005"},{"key":"e_1_3_3_10_2","doi-asserted-by":"publisher","DOI":"10.3389\/fneur.2014.00005"},{"key":"e_1_3_3_11_2","doi-asserted-by":"publisher","DOI":"10.1097\/01.HTR.0000341437.59627.ec"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1089\/neu.2010.1729"},{"key":"e_1_3_3_13_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.expneurol.2012.09.012"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1002\/jnr.21677"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.21-06-02113.2001"},{"key":"e_1_3_3_16_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0896-6273(04)00144-8"},{"key":"e_1_3_3_17_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0092-8674(00)81387-2"},{"key":"e_1_3_3_18_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0301-0082(96)00069-X"},{"key":"e_1_3_3_19_2","doi-asserted-by":"publisher","DOI":"10.1177\/1073858408315026"},{"key":"e_1_3_3_20_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.21-24-09713.2001"},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.22-07-02469.2002"},{"key":"e_1_3_3_22_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.22-08-03033.2002"},{"key":"e_1_3_3_23_2","doi-asserted-by":"publisher","DOI":"10.1016\/0031-9384(81)90221-3"},{"key":"e_1_3_3_24_2","doi-asserted-by":"publisher","DOI":"10.1016\/0031-9384(71)90218-6"},{"key":"e_1_3_3_25_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0091-6773(72)80174-3"},{"key":"e_1_3_3_26_2","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1097-4695(199608)30:4<521::AID-NEU7>3.0.CO;2-5"},{"key":"e_1_3_3_27_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2007.05.028"},{"key":"e_1_3_3_28_2","first-page":"962","article-title":"Association between injury pattern of patients with multiple injuries and circulating levels of soluble tumor necrosis factor receptors, interleukin-6 and interleukin-10, and polymorphonuclear neutrophil elastase","volume":"52","author":"Hensler T.","year":"2002","unstructured":"Hensler T., , Sauerland S., , Bouillon B., , Raum M., , Rixen D., , Helling H.J., , Andermahr J., , and Neugebauer E.A. (2002). Association between injury pattern of patients with multiple injuries and circulating levels of soluble tumor necrosis factor receptors, interleukin-6 and interleukin-10, and polymorphonuclear neutrophil elastase. J. Trauma, 52, 962\u2013970.","journal-title":"J. Trauma"},{"key":"e_1_3_3_29_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jss.2012.07.071"},{"key":"e_1_3_3_30_2","doi-asserted-by":"publisher","DOI":"10.1179\/016164108X323771"},{"key":"e_1_3_3_31_2","doi-asserted-by":"publisher","DOI":"10.1097\/00005072-199710000-00007"},{"key":"e_1_3_3_32_2","doi-asserted-by":"publisher","DOI":"10.1159\/000346155"},{"key":"e_1_3_3_33_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.17-19-07415.1997"},{"key":"e_1_3_3_34_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.peptides.2012.04.014"},{"key":"e_1_3_3_35_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.09-02-00683.1989"},{"key":"e_1_3_3_36_2","doi-asserted-by":"publisher","DOI":"10.1002\/neu.480230506"},{"key":"e_1_3_3_37_2","doi-asserted-by":"publisher","DOI":"10.1097\/01.TA.0000108998.48026.C3"},{"key":"e_1_3_3_38_2","doi-asserted-by":"publisher","DOI":"10.1089\/neu.1997.14.419"},{"key":"e_1_3_3_39_2","doi-asserted-by":"publisher","DOI":"10.1089\/neu.2009.0933"},{"key":"e_1_3_3_40_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2011.02.020"},{"key":"e_1_3_3_41_2","doi-asserted-by":"publisher","DOI":"10.1016\/0166-2236(90)90017-5"},{"key":"e_1_3_3_42_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.22-07-02679.2002"},{"key":"e_1_3_3_43_2","doi-asserted-by":"publisher","DOI":"10.1093\/chemse\/bjp038"},{"key":"e_1_3_3_44_2","doi-asserted-by":"publisher","DOI":"10.1097\/00002727-200011000-00002"},{"key":"e_1_3_3_45_2","doi-asserted-by":"publisher","DOI":"10.1097\/00002727-200011000-00003"},{"key":"e_1_3_3_46_2","first-page":"1113","article-title":"Plasma membrane damage as a marker of neuronal injury","volume":"2009","author":"LaPlaca M.C.","year":"2009","unstructured":"LaPlaca M.C., , Prado G.R., , Cullen D., , and Simon C.M. (2009). Plasma membrane damage as a marker of neuronal injury. Conf. Proc. IEEE Eng. Med. Biol. Soc., 2009, 1113\u20131116.","journal-title":"Conf. Proc. IEEE Eng. Med. Biol. Soc."},{"key":"e_1_3_3_47_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0165-0173(02)00141-8"},{"key":"e_1_3_3_48_2","doi-asserted-by":"publisher","DOI":"10.1023\/A:1022453332560"},{"key":"e_1_3_3_49_2","first-page":"85","article-title":"Cerebrovascular pathophysiology following mild traumatic brain injury","volume":"31","author":"Len T.K.","year":"2011","unstructured":"Len T.K., , and Neary J.P. (2011). Cerebrovascular pathophysiology following mild traumatic brain injury. Clin. Physiol. Funct. Imaging, 31, 85\u201393.","journal-title":"Clin. Physiol. Funct. Imaging"},{"key":"e_1_3_3_50_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1471-4159.1998.70062377.x"},{"key":"e_1_3_3_51_2","doi-asserted-by":"publisher","DOI":"10.1089\/neu.1999.16.555"},{"key":"e_1_3_3_52_2","doi-asserted-by":"publisher","DOI":"10.1089\/neu.2009.1196"},{"key":"e_1_3_3_53_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1460-9568.2006.05275.x"},{"key":"e_1_3_3_54_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2004.06.046"},{"key":"e_1_3_3_55_2","first-page":"8","article-title":"Posttraumatic anosmia in craniofacial trauma","volume":"3","author":"Jimenez D.F.","year":"1997","unstructured":"Jimenez D.F., , Sundrani S., , and Barone C.M. (1997). Posttraumatic anosmia in craniofacial trauma. J. Craniomaxillofac. Trauma, 3, 8\u201315.","journal-title":"J. Craniomaxillofac. Trauma"},{"key":"e_1_3_3_56_2","doi-asserted-by":"publisher","DOI":"10.4076\/1752-1947-3-9283"},{"key":"e_1_3_3_57_2","doi-asserted-by":"publisher","DOI":"10.1089\/neu.2009.0894"},{"key":"e_1_3_3_58_2","first-page":"306","article-title":"[Two cases of traumatic anosmia without fracture of the cranial base]","volume":"29","author":"Giraud J.C.","year":"1957","unstructured":"Giraud J.C., , Lebon P., , and Zenou M. (1957). [Two cases of traumatic anosmia without fracture of the cranial base]. Rev. Otoneuroophtalmol., 29, 306\u2013307.","journal-title":"Rev. Otoneuroophtalmol."},{"key":"e_1_3_3_59_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0009-8981(02)00330-3"},{"key":"e_1_3_3_60_2","doi-asserted-by":"publisher","DOI":"10.1212\/01.WNL.0000120550.00643.DC"},{"key":"e_1_3_3_61_2","doi-asserted-by":"publisher","DOI":"10.1089\/08977150260337967"},{"key":"e_1_3_3_62_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0079-6123(08)63270-7"},{"key":"e_1_3_3_63_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.expneurol.2005.10.011"},{"key":"e_1_3_3_64_2","doi-asserted-by":"publisher","DOI":"10.1002\/stem.1516"},{"key":"e_1_3_3_65_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1471-4159.2005.03362.x"},{"key":"e_1_3_3_66_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0079-6123(08)00446-9"},{"key":"e_1_3_3_67_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbrc.2009.09.015"},{"key":"e_1_3_3_68_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2012.11.028"},{"key":"e_1_3_3_69_2","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.3003748"},{"key":"e_1_3_3_70_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0166-2236(96)10072-2"},{"key":"e_1_3_3_71_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.expneurol.2006.04.013"},{"key":"e_1_3_3_72_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.2805-06.2006"},{"key":"e_1_3_3_73_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.1717-10.2010"},{"key":"e_1_3_3_74_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2008.04.044"},{"key":"e_1_3_3_75_2","doi-asserted-by":"publisher","DOI":"10.1089\/089771503770802871"},{"key":"e_1_3_3_76_2","doi-asserted-by":"publisher","DOI":"10.1186\/1742-2094-8-78"},{"key":"e_1_3_3_77_2","doi-asserted-by":"publisher","DOI":"10.1186\/1742-2094-6-32"},{"key":"e_1_3_3_78_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.22-03-00629.2002"},{"key":"e_1_3_3_79_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1460-9568.1991.tb00081.x"},{"key":"e_1_3_3_80_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.expneurol.2007.06.022"},{"key":"e_1_3_3_81_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.18-19-07768.1998"},{"key":"e_1_3_3_82_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.081011098"},{"key":"e_1_3_3_83_2","doi-asserted-by":"publisher","DOI":"10.1161\/01.STR.32.8.1890"},{"key":"e_1_3_3_84_2","doi-asserted-by":"publisher","DOI":"10.3233\/RNN-2007-00369"},{"key":"e_1_3_3_85_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2004.04.079"},{"key":"e_1_3_3_86_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2009.04.042"},{"key":"e_1_3_3_87_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.expneurol.2005.09.004"},{"key":"e_1_3_3_88_2","doi-asserted-by":"publisher","DOI":"10.1089\/neu.2006.0255"},{"key":"e_1_3_3_89_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2009.06.045"}],"container-title":["Journal of Neurotrauma"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.sagepub.com\/doi\/full-xml\/10.1089\/neu.2013.3296","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.sagepub.com\/doi\/pdf\/10.1089\/neu.2013.3296","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.sagepub.com\/doi\/pdf\/10.1089\/neu.2013.3296","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,1]],"date-time":"2026-05-01T22:19:52Z","timestamp":1777673992000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.sagepub.com\/doi\/full\/10.1089\/neu.2013.3296"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2014,7]]},"references-count":88,"journal-issue":{"issue":"14","published-print":{"date-parts":[[2014,7]]}},"alternative-id":["10.1089\/neu.2013.3296"],"URL":"https:\/\/doi.org\/10.1089\/neu.2013.3296","relation":{},"ISSN":["0897-7151","1557-9042"],"issn-type":[{"value":"0897-7151","type":"print"},{"value":"1557-9042","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,7]]}}}