{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T14:51:34Z","timestamp":1788274294806,"version":"build-2803163510"},"reference-count":56,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2019,12,1]],"date-time":"2019-12-01T00:00:00Z","timestamp":1575158400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2019,12,1]],"date-time":"2019-12-01T00:00:00Z","timestamp":1575158400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"}],"funder":[{"DOI":"10.13039\/100005191","name":"Craig H. Neilsen Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100005191","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["clinicalkey.com","clinicalkey.com.au","clinicalkey.es","clinicalkey.fr","clinicalkey.jp","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Physiology &amp; Behavior"],"published-print":{"date-parts":[[2019,12]]},"DOI":"10.1016\/j.physbeh.2019.112695","type":"journal-article","created":{"date-parts":[[2019,10,21]],"date-time":"2019-10-21T12:18:04Z","timestamp":1571660284000},"page":"112695","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":10,"special_numbering":"C","title":["A brief period of moderate noxious stimulation induces hemorrhage and impairs locomotor recovery after spinal cord injury"],"prefix":"10.1016","volume":"212","author":[{"given":"Misty M.","family":"Strain","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle A.","family":"Hook","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joshua D.","family":"Reynolds","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yung-Jen","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melissa K.","family":"Henwood","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James W.","family":"Grau","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"issue":"2","key":"10.1016\/j.physbeh.2019.112695_bib0001","doi-asserted-by":"crossref","first-page":"281","DOI":"10.55782\/ane-2011-1848","article-title":"Secondary injury mechanisms in traumatic spinal cord injury: a nugget of this multiply cascade","volume":"71","author":"Oyinbo","year":"2011","journal-title":"Acta Neurobiol. Exp. (Wars)"},{"key":"10.1016\/j.physbeh.2019.112695_bib0002","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.expneurol.2018.09.018","article-title":"Engaging pain fibers after a spinal cord injury fosters hemorrhage and expands the area of secondary injury","volume":"311","author":"Turtle","year":"2019","journal-title":"Exp. Neurol."},{"issue":"6","key":"10.1016\/j.physbeh.2019.112695_bib0003","doi-asserted-by":"crossref","first-page":"1200","DOI":"10.1089\/neu.2016.4778","article-title":"Pain input impairs recovery after spinal cord injury: treatment with lidocaine","volume":"34","author":"Turtle","year":"2017","journal-title":"J. Neurotrauma"},{"key":"10.1016\/j.physbeh.2019.112695_bib0004","doi-asserted-by":"crossref","first-page":"27","DOI":"10.3389\/fnsys.2018.00027","article-title":"Pain input after spinal cord injury (SCI) undermines long-term recovery and engages signal pathways that promote cell death","volume":"12","author":"Turtle","year":"2018","journal-title":"Front. Syst. Neurosci."},{"key":"10.1016\/j.physbeh.2019.112695_bib0005","series-title":"Spinal Cord Injury Facts and Figures at a Glance, in Annual Statistical Report for the Spinal Cord Injury Model Systems Public Version","first-page":"1","year":"2016"},{"issue":"5944","key":"10.1016\/j.physbeh.2019.112695_bib0006","doi-asserted-by":"crossref","first-page":"686","DOI":"10.1038\/306686a0","article-title":"Evidence for a central component of post-injury pain hypersensitivity","volume":"306","author":"Woolf","year":"1983","journal-title":"Nature"},{"issue":"11","key":"10.1016\/j.physbeh.2019.112695_bib0007","doi-asserted-by":"crossref","first-page":"2344","DOI":"10.1016\/j.pain.2014.08.034","article-title":"Peripheral noxious stimulation reduces withdrawal threshold to mechanical stimuli after spinal cord injury: role of tumor necrosis factor alpha and apoptosis","volume":"155","author":"Garraway","year":"2014","journal-title":"Pain"},{"issue":"12","key":"10.1016\/j.physbeh.2019.112695_bib0008","doi-asserted-by":"crossref","first-page":"1795","DOI":"10.1089\/neu.2004.21.1795","article-title":"Uncontrollable stimulation undermines recovery after spinal cord injury","volume":"21","author":"Grau","year":"2004","journal-title":"J. Neurotrauma"},{"key":"10.1016\/j.physbeh.2019.112695_bib0009","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.nlm.2013.08.003","article-title":"Learning from the spinal cord: how the study of spinal cord plasticity informs our view of learning","volume":"108","author":"Grau","year":"2014","journal-title":"Neurobiol. Learn. Mem."},{"key":"10.1016\/j.physbeh.2019.112695_bib0010","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.nlm.2018.04.007","article-title":"Metaplasticity within the spinal cord: evidence brain-derived neurotrophic factor (BDNF), tumor necrosis factor (TNF), and alterations in gaba function (ionic plasticity) modulate pain and the capacity to learn","volume":"154","author":"Grau","year":"2018","journal-title":"Neurobiol. Learn. Mem."},{"issue":"10","key":"10.1016\/j.physbeh.2019.112695_bib0011","doi-asserted-by":"crossref","first-page":"1873","DOI":"10.1089\/neu.2016.4626","article-title":"When pain hurts: nociceptive stimulation induces a state of maladaptive plasticity and impairs recovery after spinal cord injury","volume":"34","author":"Grau","year":"2017","journal-title":"J. Neurotrauma"},{"issue":"4","key":"10.1016\/j.physbeh.2019.112695_bib0012","doi-asserted-by":"crossref","first-page":"1030","DOI":"10.1016\/j.neuroscience.2008.07.003","article-title":"Timing in the absence of supraspinal input I: variable, but not fixed, spaced stimulation of the sciatic nerve undermines spinally-mediated instrumental learning","volume":"155","author":"Baumbauer","year":"2008","journal-title":"Neuroscience"},{"issue":"1","key":"10.1016\/j.physbeh.2019.112695_bib0013","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1037\/0735-7044.122.1.233","article-title":"Peripheral inflammation undermines the plasticity of the isolated spinal cord","volume":"122","author":"Hook","year":"2008","journal-title":"Behav. Neurosci."},{"issue":"8","key":"10.1016\/j.physbeh.2019.112695_bib0014","doi-asserted-by":"crossref","first-page":"2105","DOI":"10.1172\/JCI32041","article-title":"Endothelial sulfonylurea receptor 1-regulated nc ca-atp channels mediate progressive hemorrhagic necrosis following spinal cord injury","volume":"117","author":"Simard","year":"2007","journal-title":"J. Clin. Invest."},{"issue":"6","key":"10.1016\/j.physbeh.2019.112695_bib0015","doi-asserted-by":"crossref","first-page":"1032","DOI":"10.1037\/0735-7044.116.6.1032","article-title":"Instrumental learning within the spinal cord: IV. Induction and retention of the behavioral deficit observed after noncontingent shock","volume":"116","author":"Crown","year":"2002","journal-title":"Behav. Neurosci."},{"key":"10.1016\/j.physbeh.2019.112695_bib0016","unstructured":"Council, N.R. and I.f.L.A. Research, Guide for the care and use of laboratory animals, in committee for the update of the guide for the care and use of laboratory animals., N.A. Press, Editor. 2011, National Academies Press,: Washington, D.C.p. xxv, 220 p."},{"issue":"1","key":"10.1016\/j.physbeh.2019.112695_bib0017","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1089\/neu.1995.12.1","article-title":"A sensitive and reliable locomotor rating scale for open field testing in rats","volume":"12","author":"Basso","year":"1995","journal-title":"J. Neurotrauma"},{"issue":"11","key":"10.1016\/j.physbeh.2019.112695_bib0018","doi-asserted-by":"crossref","first-page":"1601","DOI":"10.1089\/neu.2004.21.1601","article-title":"A simple post hoc transformation that improves the metric properties of the bbb scale for rats with moderate to severe spinal cord injury","volume":"21","author":"Ferguson","year":"2004","journal-title":"J. Neurotrauma"},{"key":"10.1016\/j.physbeh.2019.112695_bib0019","unstructured":"Prahl, S.Optical absorption of hemoglobin. 1999 September1, 2018 [cited 2019 May 16]."},{"key":"10.1016\/j.physbeh.2019.112695_bib0020","article-title":"Response Suppression, in Punishment and Aversion Behavior","author":"Church","year":"1969"},{"issue":"4","key":"10.1016\/j.physbeh.2019.112695_bib0021","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1037\/0097-7403.21.4.331","article-title":"Impact of shock on pain reactivity: I. whether hypo- or hyperalgesia is observed depends on how pain reactivity is tested","volume":"21","author":"Illich","year":"1995","journal-title":"J. Exp. Psychol. Anim. Behav. Process."},{"issue":"3","key":"10.1016\/j.physbeh.2019.112695_bib0022","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1037\/0097-7403.22.3.265","article-title":"Impact of shock on pain reactivity: ii. Evidence for enhanced pain","volume":"22","author":"King","year":"1996","journal-title":"J. Exp. Psychol. Anim. Behav. Process."},{"key":"10.1016\/j.physbeh.2019.112695_bib0023","article-title":"Psychophysics of Punishment, in Punishment and Aversive Behavior","author":"Campbell","year":"1969"},{"issue":"1","key":"10.1016\/j.physbeh.2019.112695_bib0024","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1016\/j.neuroscience.2006.03.029","article-title":"Nociceptive plasticity inhibits adaptive learning in the spinal cord","volume":"141","author":"Ferguson","year":"2006","journal-title":"Neuroscience"},{"key":"10.1016\/j.physbeh.2019.112695_bib0025","doi-asserted-by":"crossref","first-page":"399","DOI":"10.3389\/fphys.2012.00399","article-title":"Maladaptive spinal plasticity opposes spinal learning and recovery in spinal cord injury","volume":"3","author":"Ferguson","year":"2012","journal-title":"Front. Physiol."},{"issue":"6","key":"10.1016\/j.physbeh.2019.112695_bib0026","doi-asserted-by":"crossref","first-page":"1366","DOI":"10.1037\/0735-7044.112.6.1366","article-title":"Instrumental learning within the spinal cord: I. Behavioral properties","volume":"112","author":"Grau","year":"1998","journal-title":"Behav. Neurosci."},{"key":"10.1016\/j.physbeh.2019.112695_bib0027","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1111\/j.1749-6632.2001.tb05821.x","article-title":"Role of neurotransmitters in sensitization of pain responses","volume":"933","author":"Willis","year":"2001","journal-title":"Ann. N. Y. Acad. Sci."},{"issue":"6","key":"10.1016\/j.physbeh.2019.112695_bib0028","doi-asserted-by":"crossref","first-page":"e39751","DOI":"10.1371\/journal.pone.0039751","article-title":"Glial tumor necrosis factor alpha (TNFalpha) generates metaplastic inhibition of spinal learning","volume":"7","author":"Huie","year":"2012","journal-title":"PLoS One"},{"issue":"5","key":"10.1016\/j.physbeh.2019.112695_bib0029","doi-asserted-by":"crossref","DOI":"10.1523\/ENEURO.0091-15.2015","article-title":"AMPA receptor phosphorylation and synaptic colocalization on motor neurons drive maladaptive plasticity below complete spinal cord injury","volume":"2","author":"Huie","year":"2015","journal-title":"eNeuro"},{"issue":"6","key":"10.1016\/j.physbeh.2019.112695_bib0030","doi-asserted-by":"crossref","first-page":"1032","DOI":"10.1037\/0735-7044.116.6.1032","article-title":"Instrumental learning within the spinal cord: IV. Induction and retention of the behavioral deficit observed after noncontingent shock","volume":"116","author":"Crown","year":"2002","journal-title":"Behav. Neurosci."},{"key":"10.1016\/j.physbeh.2019.112695_bib0031","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.expneurol.2018.09.018","article-title":"Engaging pain fibers after a spinal cord injury fosters hemorrhage and expands the area of secondary injury","volume":"311","author":"Turtle","year":"2019","journal-title":"Exp. Neurol."},{"key":"10.1016\/j.physbeh.2019.112695_bib0032","first-page":"A","article-title":"Inflammatory response to peripheral pain input after SCI is blocked by a spinal transection","volume":"34","author":"Reynolds","year":"2017","journal-title":"J. Neurotrauma"},{"issue":"Suppl4","key":"10.1016\/j.physbeh.2019.112695_bib0033","article-title":"The sur1-trpm4 channel in spinal cord injury","author":"Simard","year":"2013","journal-title":"J. Spine"},{"issue":"1","key":"10.1016\/j.physbeh.2019.112695_bib0034","doi-asserted-by":"crossref","first-page":"71","DOI":"10.3758\/BF03331957","article-title":"The relationship between shock severity and the form of the antinociception observed in pentobarbital-anesthetized rats","volume":"24","author":"Grau","year":"1996","journal-title":"Psychobiology"},{"issue":"3","key":"10.1016\/j.physbeh.2019.112695_bib0035","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1037\/0735-7044.107.3.493","article-title":"Activation of the opioid and nonopioid hypoalgesic systems at the level of the brainstem and spinal cord: does a coulometric relation predict the emergence or form of environmentally induced hypoalgesia?","volume":"107","author":"Meagher","year":"1993","journal-title":"Behav. Neurosci."},{"issue":"4","key":"10.1016\/j.physbeh.2019.112695_bib0036","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1037\/h0040896","article-title":"A scale of apparent intensity of electric shock","volume":"56","author":"Stevens","year":"1958","journal-title":"J. Exp. Psychol."},{"key":"10.1016\/j.physbeh.2019.112695_bib0037","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1037\/h0045795","article-title":"The surprising simplicity of sensory metrics","volume":"17","author":"Stevens","year":"1962","journal-title":"Am. Psychol."},{"issue":"1","key":"10.1016\/j.physbeh.2019.112695_bib0038","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/j.expneurol.2005.07.016","article-title":"Evidence that descending serotonergic systems protect spinal cord plasticity against the disruptive effect of uncontrollable stimulation","volume":"196","author":"Crown","year":"2005","journal-title":"Exp. Neurol."},{"issue":"3","key":"10.1016\/j.physbeh.2019.112695_bib0039","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/S0304-3959(00)00448-6","article-title":"Induction of long-term potentiation of single wide dynamic range neurones in the dorsal horn is inhibited by descending pathways","volume":"91","author":"Gjerstad","year":"2001","journal-title":"Pain"},{"key":"10.1016\/j.physbeh.2019.112695_bib0040","first-page":"A48","article-title":"Pain induced hemorrhage after spinal cord injury is blocked by lidocaine applied rostrally to injury","volume":"35","author":"Davis","year":"2018","journal-title":"J. Neurotrauma"},{"key":"10.1016\/j.physbeh.2019.112695_bib0041","first-page":"A","article-title":"Pain induced hemorrhage after spinal cord injury is blocked by pentobarbital anesthesia","volume":"34","author":"Davis","year":"2017","journal-title":"J. Neurotrauma"},{"issue":"3","key":"10.1016\/j.physbeh.2019.112695_bib0042","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1161\/01.STR.20.3.372","article-title":"Spinal cord blood flow and systemic blood pressure after experimental spinal cord injury in rats","volume":"20","author":"Guha","year":"1989","journal-title":"Stroke"},{"issue":"21","key":"10.1016\/j.physbeh.2019.112695_bib0043","doi-asserted-by":"crossref","first-page":"1789","DOI":"10.1089\/neu.2014.3399","article-title":"Development of a database for translational spinal cord injury research","volume":"31","author":"Nielson","year":"2014","journal-title":"J. Neurotrauma"},{"key":"10.1016\/j.physbeh.2019.112695_bib0044","first-page":"A","article-title":"Noxious stimulation after spinal cord injury induces a brain- dependent increase in hemorrhage","volume":"35","author":"Fauss","year":"2018","journal-title":"J. Neurotrauma"},{"issue":"8","key":"10.1016\/j.physbeh.2019.112695_bib0045","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1089\/089771503767869944","article-title":"Autonomic dysreflexia in acute spinal cord injury: an under-recognized clinical entity","volume":"20","author":"Krassioukov","year":"2003","journal-title":"J. Neurotrauma"},{"key":"10.1016\/j.physbeh.2019.112695_bib0046","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/S0079-6123(05)52017-X","article-title":"Segmental organization of spinal reflexes mediating autonomic dysreflexia after spinal cord injury","volume":"152","author":"Rabchevsky","year":"2006","journal-title":"Prog. Brain Res."},{"issue":"6","key":"10.1016\/j.physbeh.2019.112695_bib0047","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1007\/s10286-002-0076-0","article-title":"What causes autonomic dysreflexia after spinal cord injury?","volume":"12","author":"Weaver","year":"2002","journal-title":"Clin. Auton. Res."},{"issue":"11","key":"10.1016\/j.physbeh.2019.112695_bib0048","doi-asserted-by":"crossref","first-page":"702","DOI":"10.1038\/sj.sc.3102096","article-title":"An animal model of functional electrical stimulation: evidence that the central nervous system modulates the consequences of training","volume":"45","author":"Hook","year":"2007","journal-title":"Spinal Cord"},{"issue":"3","key":"10.1016\/j.physbeh.2019.112695_bib0049","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1177\/1545968314543500","article-title":"Hindlimb stretching alters locomotor function after spinal cord injury in the adult rat","volume":"29","author":"Caudle","year":"2015","journal-title":"Neurorehabil. Neural Repair"},{"issue":"3","key":"10.1016\/j.physbeh.2019.112695_bib0050","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1089\/neu.2015.4227","article-title":"Disruption of locomotion in response to hindlimb muscle stretch at acute and chronic time points after a spinal cord injury in rats","volume":"34","author":"Keller","year":"2017","journal-title":"J. Neurotrauma"},{"issue":"12","key":"10.1016\/j.physbeh.2019.112695_bib0051","doi-asserted-by":"crossref","first-page":"2086","DOI":"10.1089\/neu.2016.4951","article-title":"Dynamic \"Range of motion\" hindlimb stretching disrupts locomotor function in rats with moderate subacute spinal cord injuries","volume":"34","author":"Keller","year":"2017","journal-title":"J. Neurotrauma"},{"issue":"8","key":"10.1016\/j.physbeh.2019.112695_bib0052","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1177\/1545968311407519","article-title":"Hindlimb immobilization in a wheelchair alters functional recovery following contusive spinal cord injury in the adult rat","volume":"25","author":"Caudle","year":"2011","journal-title":"Neurorehabil. Neural Repair"},{"issue":"2","key":"10.1016\/j.physbeh.2019.112695_bib0053","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/j.bbr.2007.02.035","article-title":"The impact of morphine after a spinal cord injury","volume":"179","author":"Hook","year":"2007","journal-title":"Behav. Brain Res."},{"issue":"5","key":"10.1016\/j.physbeh.2019.112695_bib0054","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1089\/neu.2008.0710","article-title":"Intrathecal morphine attenuates recovery of function after a spinal cord injury","volume":"26","author":"Hook","year":"2009","journal-title":"J. Neurotrauma"},{"issue":"8","key":"10.1016\/j.physbeh.2019.112695_bib0055","doi-asserted-by":"crossref","first-page":"e71317","DOI":"10.1371\/journal.pone.0071317","article-title":"Systematic review and meta-analysis of therapeutic hypothermia in animal models of spinal cord injury","volume":"8","author":"Batchelor","year":"2013","journal-title":"PLoS One"},{"issue":"28","key":"10.1016\/j.physbeh.2019.112695_bib0056","doi-asserted-by":"crossref","first-page":"9190","DOI":"10.1523\/JNEUROSCI.5303-13.2014","article-title":"Tonic pain experienced during locomotor training impairs retention despite normal performance during acquisition","volume":"34","author":"Bouffard","year":"2014","journal-title":"J. Neurosci."}],"container-title":["Physiology &amp; Behavior"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0031938419305189?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0031938419305189?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,21]],"date-time":"2025-09-21T18:10:34Z","timestamp":1758478234000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0031938419305189"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12]]},"references-count":56,"alternative-id":["S0031938419305189"],"URL":"https:\/\/doi.org\/10.1016\/j.physbeh.2019.112695","relation":{},"ISSN":["0031-9384"],"issn-type":[{"value":"0031-9384","type":"print"}],"subject":[],"published":{"date-parts":[[2019,12]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"A brief period of moderate noxious stimulation induces hemorrhage and impairs locomotor recovery after spinal cord injury","name":"articletitle","label":"Article Title"},{"value":"Physiology & Behavior","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.physbeh.2019.112695","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2019 Elsevier Inc. All rights reserved.","name":"copyright","label":"Copyright"}],"article-number":"112695"}}