{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T01:58:23Z","timestamp":1791597503384,"version":"4.3.4"},"reference-count":95,"publisher":"Elsevier BV","issue":"4","license":[{"start":{"date-parts":[[2017,2,1]],"date-time":"2017-02-01T00:00:00Z","timestamp":1485907200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2018,2,23]],"date-time":"2018-02-23T00:00:00Z","timestamp":1519344000000},"content-version":"vor","delay-in-days":387,"URL":"http:\/\/www.elsevier.com\/open-access\/userlicense\/1.0\/"}],"funder":[{"name":"NIH\/NIDA","award":["DA031777"],"award-info":[{"award-number":["DA031777"]}]},{"DOI":"10.13039\/100001447","name":"Rita Allen Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100001447","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009658","name":"American Pain Society","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009658","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Stanford Dean\u2019s fellowship"},{"name":"HHMI medical research fellowship"},{"name":"NDSEG fellowship"},{"DOI":"10.13039\/100000011","name":"HHMI","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000011","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["cell.com","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Neuron"],"published-print":{"date-parts":[[2017,2]]},"DOI":"10.1016\/j.neuron.2017.01.008","type":"journal-article","created":{"date-parts":[[2017,2,3]],"date-time":"2017-02-03T06:03:35Z","timestamp":1486101815000},"page":"822-839.e6","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":358,"title":["A Brainstem-Spinal Cord Inhibitory Circuit for Mechanical Pain Modulation by GABA and Enkephalins"],"prefix":"10.1016","volume":"93","author":[{"given":"Amaury","family":"Fran\u00e7ois","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah A.","family":"Low","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth I.","family":"Sypek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amelia J.","family":"Christensen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chaudy","family":"Sotoudeh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kevin T.","family":"Beier","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charu","family":"Ramakrishnan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kimberly D.","family":"Ritola","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Reza","family":"Sharif-Naeini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karl","family":"Deisseroth","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Scott L.","family":"Delp","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert C.","family":"Malenka","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liqun","family":"Luo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam W.","family":"Hantman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gr\u00e9gory","family":"Scherrer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.neuron.2017.01.008_bib1","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1016\/j.neuron.2013.07.051","article-title":"The sensory neurons of touch","volume":"79","author":"Abraira","year":"2013","journal-title":"Neuron"},{"key":"10.1016\/j.neuron.2017.01.008_bib2","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1016\/0306-4522(96)00063-2","article-title":"Direct evidence of an extensive GABAergic innervation of the spinal dorsal horn by fibres descending from the rostral ventromedial medulla","volume":"73","author":"Antal","year":"1996","journal-title":"Neuroscience"},{"key":"10.1016\/j.neuron.2017.01.008_bib3","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/j.expneurol.2010.08.019","article-title":"Deep brain stimulation of the lateral cerebellar nucleus produces frequency-specific alterations in motor evoked potentials in the rat in\u00a0vivo","volume":"226","author":"Baker","year":"2010","journal-title":"Exp. Neurol."},{"key":"10.1016\/j.neuron.2017.01.008_bib4","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/0006-8993(86)91296-5","article-title":"Putative pain modulating neurons in the rostral ventral medulla: reflex-related activity predicts effects of morphine","volume":"366","author":"Barbaro","year":"1986","journal-title":"Brain Res."},{"key":"10.1016\/j.neuron.2017.01.008_bib5","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1111\/nyas.12056","article-title":"Pre- and postsynaptic inhibitory control in the spinal cord dorsal horn","volume":"1279","author":"Bardoni","year":"2013","journal-title":"Ann. N Y Acad. Sci."},{"key":"10.1016\/j.neuron.2017.01.008_bib6","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1016\/j.neuron.2014.01.044","article-title":"Delta opioid receptors presynaptically regulate cutaneous mechanosensory neuron input to the spinal cord dorsal horn","volume":"81","author":"Bardoni","year":"2014","journal-title":"Neuron"},{"key":"10.1016\/j.neuron.2017.01.008_bib7","doi-asserted-by":"crossref","first-page":"4685","DOI":"10.1073\/pnas.73.12.4685","article-title":"Opiate and stimulus-produced analgesia: functional anatomy of a medullospinal pathway","volume":"73","author":"Basbaum","year":"1976","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.neuron.2017.01.008_bib8","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.cell.2009.09.028","article-title":"Cellular and molecular mechanisms of pain","volume":"139","author":"Basbaum","year":"2009","journal-title":"Cell"},{"key":"10.1016\/j.neuron.2017.01.008_bib9","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1016\/j.cell.2015.07.015","article-title":"Circuit architecture of VTA dopamine neurons revealed by systematic input-output mapping","volume":"162","author":"Beier","year":"2015","journal-title":"Cell"},{"key":"10.1016\/j.neuron.2017.01.008_bib10","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1016\/0006-8993(83)90994-0","article-title":"Immunohistochemical evidence for the presence of gamma-aminobutyric acid and serotonin in one nerve cell. A study on the raphe nuclei of the rat using antibodies to glutamate decarboxylase and serotonin","volume":"275","author":"Belin","year":"1983","journal-title":"Brain Res."},{"key":"10.1016\/j.neuron.2017.01.008_bib11","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1016\/S0306-4522(97)00399-0","article-title":"Swim-stress but not opioid withdrawal increases expression of c-fos immunoreactivity in rat periaqueductal gray neurons which project to the rostral ventromedial medulla","volume":"83","author":"Bellchambers","year":"1998","journal-title":"Neuroscience"},{"key":"10.1016\/j.neuron.2017.01.008_bib12","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.cell.2009.08.027","article-title":"Stringent specificity in the construction of a GABAergic presynaptic inhibitory circuit","volume":"139","author":"Betley","year":"2009","journal-title":"Cell"},{"key":"10.1016\/j.neuron.2017.01.008_bib13","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1016\/j.cell.2015.01.011","article-title":"Identification of a spinal circuit for light touch and fine motor control","volume":"160","author":"Bourane","year":"2015","journal-title":"Cell"},{"key":"10.1016\/j.neuron.2017.01.008_bib14","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1016\/S0896-6273(00)81205-2","article-title":"Adaptive rescaling maximizes information transmission","volume":"26","author":"Brenner","year":"2000","journal-title":"Neuron"},{"key":"10.1016\/j.neuron.2017.01.008_bib15","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1152\/jn.1998.79.2.677","article-title":"Endogenous opioid peptides acting at mu-opioid receptors in the dorsal horn contribute to midbrain modulation of spinal nociceptive neurons","volume":"79","author":"Budai","year":"1998","journal-title":"J.\u00a0Neurophysiol."},{"key":"10.1016\/j.neuron.2017.01.008_bib16","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1016\/j.pneurobio.2009.04.003","article-title":"Stress-induced analgesia","volume":"88","author":"Butler","year":"2009","journal-title":"Prog. Neurobiol."},{"key":"10.1016\/j.neuron.2017.01.008_bib17","doi-asserted-by":"crossref","first-page":"9075","DOI":"10.1073\/pnas.0901507106","article-title":"Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli","volume":"106","author":"Cavanaugh","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.neuron.2017.01.008_bib18","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/0165-0270(94)90144-9","article-title":"Quantitative assessment of tactile allodynia in the rat paw","volume":"53","author":"Chaplan","year":"1994","journal-title":"J.\u00a0Neurosci. Methods"},{"key":"10.1016\/j.neuron.2017.01.008_bib19","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.neuroscience.2013.12.008","article-title":"Birth-date dependent arrangement of spinal enkephalinergic neurons: evidence from the preproenkephalin-green fluorescent protein transgenic mice","volume":"260","author":"Chen","year":"2014","journal-title":"Neuroscience"},{"key":"10.1016\/j.neuron.2017.01.008_bib20","doi-asserted-by":"crossref","first-page":"1699","DOI":"10.1016\/j.celrep.2016.10.010","article-title":"In\u00a0vivo interrogation of spinal mechanosensory circuits","volume":"17","author":"Christensen","year":"2016","journal-title":"Cell Rep."},{"key":"10.1016\/j.neuron.2017.01.008_bib21","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1038\/295663a0","article-title":"Primary structure of the human Met- and Leu-enkephalin precursor and its mRNA","volume":"295","author":"Comb","year":"1982","journal-title":"Nature"},{"key":"10.1016\/j.neuron.2017.01.008_bib22","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1038\/nrn2993","article-title":"Molecular mechanisms of mechanotransduction in mammalian sensory neurons","volume":"12","author":"Delmas","year":"2011","journal-title":"Nat. Rev. Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib23","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.brainres.2009.05.001","article-title":"Differential mediation of descending pain facilitation and inhibition by spinal 5HT-3 and 5HT-7 receptors","volume":"1280","author":"Dogrul","year":"2009","journal-title":"Brain Res."},{"key":"10.1016\/j.neuron.2017.01.008_bib24","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1016\/j.cell.2014.11.003","article-title":"Identification of spinal circuits transmitting and gating mechanical pain","volume":"159","author":"Duan","year":"2014","journal-title":"Cell"},{"key":"10.1016\/j.neuron.2017.01.008_bib25","first-page":"115","article-title":"Hyperpolarization of substantia gelatinosa neurons evoked by mu-, kappa-, delta 1-, and delta 2-selective opioids","volume":"3","author":"Eckert","year":"2002","journal-title":"J.\u00a0Pain"},{"key":"10.1016\/j.neuron.2017.01.008_bib26","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1007\/s00429-014-0717-9","article-title":"A mu-delta opioid receptor brain atlas reveals neuronal co-occurrence in subcortical networks","volume":"220","author":"Erbs","year":"2015","journal-title":"Brain Struct. Funct."},{"key":"10.1016\/j.neuron.2017.01.008_bib27","doi-asserted-by":"crossref","first-page":"2545","DOI":"10.1523\/JNEUROSCI.03-12-02545.1983","article-title":"The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat","volume":"3","author":"Fields","year":"1983","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib28","doi-asserted-by":"crossref","first-page":"684","DOI":"10.1038\/306684a0","article-title":"Evidence that disinhibition of brain stem neurones contributes to morphine analgesia","volume":"306","author":"Fields","year":"1983","journal-title":"Nature"},{"key":"10.1016\/j.neuron.2017.01.008_bib29","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1038\/nature13276","article-title":"Presynaptic inhibition of spinal sensory feedback ensures smooth movement","volume":"509","author":"Fink","year":"2014","journal-title":"Nature"},{"key":"10.1016\/j.neuron.2017.01.008_bib30","doi-asserted-by":"crossref","first-page":"1289","DOI":"10.1016\/j.neuron.2015.02.028","article-title":"Targeted ablation, silencing, and activation establish glycinergic dorsal horn neurons as key components of a spinal gate for pain and itch","volume":"85","author":"Foster","year":"2015","journal-title":"Neuron"},{"key":"10.1016\/j.neuron.2017.01.008_bib31","doi-asserted-by":"crossref","first-page":"4917","DOI":"10.1523\/JNEUROSCI.2514-15.2016","article-title":"On the role of the pedunculopontine nucleus and mesencephalic reticular formation in locomotion in nonhuman primates","volume":"36","author":"Goetz","year":"2016","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib32","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1126\/science.343250","article-title":"Endorphins: naloxone fails to alter experimental pain or mood in humans","volume":"199","author":"Grevert","year":"1978","journal-title":"Science"},{"key":"10.1016\/j.neuron.2017.01.008_bib33","doi-asserted-by":"crossref","first-page":"1646","DOI":"10.1523\/JNEUROSCI.14-03-01646.1994","article-title":"mu-Opioid agonists inhibit spinal trigeminal substantia gelatinosa neurons in guinea pig and rat","volume":"14","author":"Grudt","year":"1994","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib34","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1002\/cne.902580202","article-title":"Localization of preproenkephalin mRNA in the rat brain and spinal cord by in\u00a0situ hybridization","volume":"258","author":"Harlan","year":"1987","journal-title":"J.\u00a0Comp. Neurol."},{"key":"10.1016\/j.neuron.2017.01.008_bib35","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S0022-3565(25)23681-3","article-title":"[3H]-[H-D-Phe-Cys-Tyr-D-Trp-Orn-Thr-Pen-Thr-NH2] ([3H]CTOP), a potent and highly selective peptide for mu opioid receptors in rat brain","volume":"248","author":"Hawkins","year":"1989","journal-title":"J.\u00a0Pharmacol. Exp. Ther."},{"key":"10.1016\/j.neuron.2017.01.008_bib36","doi-asserted-by":"crossref","first-page":"1313","DOI":"10.1523\/JNEUROSCI.4060-10.2011","article-title":"Multiple targets of \u03bc-opioid receptor-mediated presynaptic inhibition at primary afferent A\u03b4- and C-fibers","volume":"31","author":"Heinke","year":"2011","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib37","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1016\/0306-4522(92)90400-V","article-title":"Direct and indirect actions of morphine on medullary neurons that modulate nociception","volume":"48","author":"Heinricher","year":"1992","journal-title":"Neuroscience"},{"key":"10.1016\/j.neuron.2017.01.008_bib38","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.brainresrev.2008.12.009","article-title":"Descending control of nociception: Specificity, recruitment and plasticity","volume":"60","author":"Heinricher","year":"2009","journal-title":"Brain Res. Brain Res. Rev."},{"key":"10.1016\/j.neuron.2017.01.008_bib39","doi-asserted-by":"crossref","first-page":"3081","DOI":"10.1073\/pnas.74.7.3081","article-title":"Immunohistochemical analysis of peptide pathways possibly related to pain and analgesia: enkephalin and substance P","volume":"74","author":"H\u00f6kfelt","year":"1977","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.neuron.2017.01.008_bib40","doi-asserted-by":"crossref","first-page":"1334","DOI":"10.1002\/ar.20755","article-title":"Preproenkephalin mRNA is expressed in a subpopulation of GABAergic neurons in the spinal dorsal horn of the GAD67-GFP knock-in mouse","volume":"291","author":"Huang","year":"2008","journal-title":"Anat. Rec. (Hoboken)"},{"key":"10.1016\/j.neuron.2017.01.008_bib41","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1038\/258577a0","article-title":"Identification of two related pentapeptides from the brain with potent opiate agonist activity","volume":"258","author":"Hughes","year":"1975","journal-title":"Nature"},{"key":"10.1016\/j.neuron.2017.01.008_bib42","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.pneurobio.2014.06.003","article-title":"Stress-induced hyperalgesia","volume":"121","author":"Jennings","year":"2014","journal-title":"Prog. Neurobiol."},{"key":"10.1016\/j.neuron.2017.01.008_bib43","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1038\/268549a0","article-title":"Opiate analgesics inhibit substance P\u00a0release from rat trigeminal nucleus","volume":"268","author":"Jessell","year":"1977","journal-title":"Nature"},{"key":"10.1016\/j.neuron.2017.01.008_bib44","doi-asserted-by":"crossref","first-page":"1787","DOI":"10.1523\/JNEUROSCI.4856-05.2006","article-title":"Direct GABAergic and glycinergic inhibition of the substantia gelatinosa from the rostral ventromedial medulla revealed by in\u00a0vivo patch-clamp analysis in rats","volume":"26","author":"Kato","year":"2006","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib45","doi-asserted-by":"crossref","first-page":"3847","DOI":"10.1038\/ncomms4847","article-title":"Chemical-genetic attenuation of focal neocortical seizures","volume":"5","author":"K\u00e4tzel","year":"2014","journal-title":"Nat. Commun."},{"key":"10.1016\/j.neuron.2017.01.008_bib46","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/S0301-0082(02)00008-4","article-title":"Exploring the opioid system by gene knockout","volume":"66","author":"Kieffer","year":"2002","journal-title":"Prog. Neurobiol."},{"key":"10.1016\/j.neuron.2017.01.008_bib47","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1101\/gr.749203","article-title":"A highly efficient recombineering-based method for generating conditional knockout mutations","volume":"13","author":"Liu","year":"2003","journal-title":"Genome Res."},{"key":"10.1016\/j.neuron.2017.01.008_bib48","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1016\/j.neulet.2014.11.008","article-title":"The coexistence of VGluT2 and neurotensin or leu-enkephalin in the medullary dorsal horn: a confocal and electron microscopic immunohistochemical study in the rat","volume":"584","author":"Liu","year":"2015","journal-title":"Neurosci. Lett."},{"key":"10.1016\/j.neuron.2017.01.008_bib49","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1113\/jphysiol.2007.131565","article-title":"Selective action of noradrenaline and serotonin on neurones of the spinal superficial dorsal horn in the rat","volume":"582","author":"Lu","year":"2007","journal-title":"J.\u00a0Physiol."},{"key":"10.1016\/j.neuron.2017.01.008_bib50","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1038\/nn.2467","article-title":"A robust and high-throughput Cre reporting and characterization system for the whole mouse brain","volume":"13","author":"Madisen","year":"2010","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib51","doi-asserted-by":"crossref","first-page":"10847","DOI":"10.1523\/JNEUROSCI.22-24-10847.2002","article-title":"Rostral ventromedial medulla neurons that project to the spinal\u00a0cord express multiple opioid receptor phenotypes","volume":"22","author":"Marinelli","year":"2002","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib52","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1002\/cne.22130","article-title":"Enkephalins, dynorphins, and beta-endorphin in the rat dorsal horn: an immunofluorescence colocalization study","volume":"517","author":"Marviz\u00f3n","year":"2009","journal-title":"J.\u00a0Comp. Neurol."},{"key":"10.1016\/j.neuron.2017.01.008_bib53","doi-asserted-by":"crossref","first-page":"21338","DOI":"10.1016\/S0021-9258(19)36614-1","article-title":"Tetanus toxin and botulinum toxins type A and B inhibit glutamate, gamma-aminobutyric acid, aspartate, and met-enkephalin release from synaptosomes. Clues to the locus of action","volume":"267","author":"McMahon","year":"1992","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1016\/j.neuron.2017.01.008_bib54","doi-asserted-by":"crossref","first-page":"1189","DOI":"10.1016\/j.neuron.2016.05.008","article-title":"Sensory-derived glutamate regulates presynaptic inhibitory terminals in mouse spinal cord","volume":"90","author":"Mende","year":"2016","journal-title":"Neuron"},{"key":"10.1016\/j.neuron.2017.01.008_bib55","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1007\/BF00176476","article-title":"Analgesia and decrement in operant performance in socially defeated mice: selective cross-tolerance to morphine and antagonism by naltrexone","volume":"92","author":"Miczek","year":"1987","journal-title":"Psychopharmacology (Berl.)"},{"key":"10.1016\/j.neuron.2017.01.008_bib56","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/0024-3205(78)90136-4","article-title":"Naloxone reversal of morphine analgesia but failure to alter reactivity to pain in the formalin test","volume":"22","author":"North","year":"1978","journal-title":"Life Sci."},{"key":"10.1016\/j.neuron.2017.01.008_bib57","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1001\/archpsyc.60.1.39","article-title":"Using chronic pain to predict depressive morbidity in the general population","volume":"60","author":"Ohayon","year":"2003","journal-title":"Arch. Gen. Psychiatry"},{"key":"10.1016\/j.neuron.2017.01.008_bib58","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.pain.2005.05.028","article-title":"Post-traumatic stress disorder symptoms, pain, and perceived life control: associations with psychosocial and physical functioning","volume":"117","author":"Palyo","year":"2005","journal-title":"Pain"},{"key":"10.1016\/j.neuron.2017.01.008_bib59","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1152\/jn.01062.2010","article-title":"Opioid receptor modulation of GABAergic and serotonergic spinally projecting neurons of the rostral ventromedial medulla in mice","volume":"106","author":"Pedersen","year":"2011","journal-title":"J.\u00a0Neurophysiol."},{"key":"10.1016\/j.neuron.2017.01.008_bib60","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1016\/j.neuron.2015.07.029","article-title":"Dorsal horn circuits for persistent mechanical pain","volume":"87","author":"Peirs","year":"2015","journal-title":"Neuron"},{"key":"10.1016\/j.neuron.2017.01.008_bib61","doi-asserted-by":"crossref","first-page":"1246","DOI":"10.1016\/j.celrep.2015.09.080","article-title":"Dorsal horn parvalbumin neurons are gate-keepers of touch-evoked pain after nerve injury","volume":"13","author":"Petitjean","year":"2015","journal-title":"Cell Rep."},{"key":"10.1016\/j.neuron.2017.01.008_bib62","doi-asserted-by":"crossref","first-page":"1226","DOI":"10.1046\/j.1471-4159.1994.63041226.x","article-title":"Expression of preproenkephalin A gene and presence of Met-enkephalin in dorsal root ganglia of the adult rat","volume":"63","author":"Pohl","year":"1994","journal-title":"J.\u00a0Neurochem."},{"key":"10.1016\/j.neuron.2017.01.008_bib63","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/S0166-2236(02)02157-4","article-title":"Chronic pain and medullary descending facilitation","volume":"25","author":"Porreca","year":"2002","journal-title":"Trends Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib64","doi-asserted-by":"crossref","first-page":"1655","DOI":"10.1523\/JNEUROSCI.14-03-01655.1994","article-title":"Serotonin immunoreactivity is contained in one physiological cell class in the rat rostral ventromedial medulla","volume":"14","author":"Potrebic","year":"1994","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib65","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1586\/ern.09.34","article-title":"Pain catastrophizing: a critical review","volume":"9","author":"Quartana","year":"2009","journal-title":"Expert Rev. Neurother."},{"key":"10.1016\/j.neuron.2017.01.008_bib66","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1007\/BF01175558","article-title":"Identification of dorsal root synaptic terminals on monkey ventral horn cells by electron microscopic autoradiography","volume":"8","author":"Ralston","year":"1979","journal-title":"J.\u00a0Neurocytol."},{"key":"10.1016\/j.neuron.2017.01.008_bib67","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1126\/science.aaf0594","article-title":"Competition between engrams influences fear memory formation and recall","volume":"353","author":"Rashid","year":"2016","journal-title":"Science"},{"key":"10.1016\/j.neuron.2017.01.008_bib68","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1002\/cne.903020213","article-title":"Contribution of brainstem GABAergic circuitry to descending antinociceptive controls: I. GABA-immunoreactive projection neurons in the periaqueductal gray and nucleus raphe magnus","volume":"302","author":"Reichling","year":"1990","journal-title":"J.\u00a0Comp. Neurol."},{"key":"10.1016\/j.neuron.2017.01.008_bib69","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1002\/cne.902810402","article-title":"Morphological characterization of substance P-like immunoreactive glomeruli in the superficial dorsal horn of the rat spinal cord and trigeminal subnucleus caudalis: a quantitative study","volume":"281","author":"Ribeiro-da-Silva","year":"1989","journal-title":"J.\u00a0Comp. Neurol."},{"key":"10.1016\/j.neuron.2017.01.008_bib70","doi-asserted-by":"crossref","first-page":"1148","DOI":"10.1016\/j.cell.2009.04.019","article-title":"Dissociation of the opioid receptor mechanisms that control mechanical and heat pain","volume":"137","author":"Scherrer","year":"2009","journal-title":"Cell"},{"key":"10.1016\/j.neuron.2017.01.008_bib71","doi-asserted-by":"crossref","first-page":"3182","DOI":"10.1021\/jm00073a020","article-title":"TIPP[psi]: a highly potent and stable pseudopeptide delta opioid receptor antagonist with extraordinary delta selectivity","volume":"36","author":"Schiller","year":"1993","journal-title":"J.\u00a0Med. Chem."},{"key":"10.1016\/j.neuron.2017.01.008_bib72","doi-asserted-by":"crossref","first-page":"5161","DOI":"10.1096\/fj.12-208678","article-title":"Pain inhibition by blocking leukocytic and neuronal opioid peptidases in peripheral inflamed tissue","volume":"26","author":"Schreiter","year":"2012","journal-title":"FASEB J."},{"key":"10.1016\/j.neuron.2017.01.008_bib73","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1038\/nature14600","article-title":"Viral-genetic tracing of the input-output organization of a central noradrenaline circuit","volume":"524","author":"Schwarz","year":"2015","journal-title":"Nature"},{"key":"10.1016\/j.neuron.2017.01.008_bib74","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1177\/28.4.6154731","article-title":"Immunohistochemical studies of peptidergic neurons in the dorsal horn of the spinal cord","volume":"28","author":"Seybold","year":"1980","journal-title":"J.\u00a0Histochem. Cytochem."},{"key":"10.1016\/j.neuron.2017.01.008_bib75","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/0306-4522(85)90225-8","article-title":"Topographic principles in the spinal projections of serotonergic and non-serotonergic brainstem neurons in the rat","volume":"15","author":"Skagerberg","year":"1985","journal-title":"Neuroscience"},{"key":"10.1016\/j.neuron.2017.01.008_bib76","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1016\/j.neuron.2016.09.021","article-title":"A designer AAV variant permits efficient retrograde access to projection neurons","volume":"92","author":"Tervo","year":"2016","journal-title":"Neuron"},{"key":"10.1016\/j.neuron.2017.01.008_bib77","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1038\/nrn2947","article-title":"Neuronal circuitry for pain processing in the dorsal horn","volume":"11","author":"Todd","year":"2010","journal-title":"Nat. Rev. Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib78","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1016\/0301-0082(93)90045-T","article-title":"The localization of classical transmitters and neuropeptides within neurons in laminae I-III of the mammalian spinal dorsal horn","volume":"41","author":"Todd","year":"1993","journal-title":"Prog. Neurobiol."},{"key":"10.1016\/j.neuron.2017.01.008_bib79","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1046\/j.1460-9568.2003.02406.x","article-title":"The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn","volume":"17","author":"Todd","year":"2003","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib80","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1038\/nn.3881","article-title":"Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing","volume":"18","author":"Usoskin","year":"2015","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib81","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1007\/s12311-010-0240-3","article-title":"Functional classification of neurons in the mouse lateral cerebellar nuclei","volume":"10","author":"Uusisaari","year":"2011","journal-title":"Cerebellum"},{"key":"10.1016\/j.neuron.2017.01.008_bib82","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1073\/pnas.1423136112","article-title":"Optogenetic activation of cholinergic neurons in the PPT or LDT induces REM sleep","volume":"112","author":"Van Dort","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.neuron.2017.01.008_bib83","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1038\/nrn3976","article-title":"The neuroscience of placebo effects: connecting context, learning and health","volume":"16","author":"Wager","year":"2015","journal-title":"Nat. Rev. Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib84","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1038\/nmeth999","article-title":"Retrograde neuronal tracing with a deletion-mutant rabies virus","volume":"4","author":"Wickersham","year":"2007","journal-title":"Nat. Methods"},{"key":"10.1016\/j.neuron.2017.01.008_bib85","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1016\/0306-4522(77)90055-0","article-title":"The direct and specific opiate-like effect of met5-enkephalin and analogues on the spinal cord","volume":"2","author":"Yaksh","year":"1977","journal-title":"Neuroscience"},{"key":"10.1016\/j.neuron.2017.01.008_bib86","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1038\/286155a0","article-title":"Intrathecal morphine inhibits substance P release from mammalian spinal cord in\u00a0vivo","volume":"286","author":"Yaksh","year":"1980","journal-title":"Nature"},{"key":"10.1016\/j.neuron.2017.01.008_bib87","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/0006-8993(83)90396-7","article-title":"Studies on the release by somatic stimulation from rat and cat spinal cord of active materials which displace dihydromorphine in an opiate-binding assay","volume":"268","author":"Yaksh","year":"1983","journal-title":"Brain Res."},{"key":"10.1016\/j.neuron.2017.01.008_bib88","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/0304-3959(93)90102-U","article-title":"Effects of intrathecal strychnine and bicuculline on nerve compression-induced thermal hyperalgesia and selective antagonism by MK-801","volume":"54","author":"Yamamoto","year":"1993","journal-title":"Pain"},{"key":"10.1016\/j.neuron.2017.01.008_bib89","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1038\/305529a0","article-title":"Substantia gelatinosa neurones hyperpolarized in\u00a0vitro by enkephalin","volume":"305","author":"Yoshimura","year":"1983","journal-title":"Nature"},{"key":"10.1016\/j.neuron.2017.01.008_bib90","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1152\/physrev.00043.2010","article-title":"Fast synaptic inhibition in spinal sensory processing and pain control","volume":"92","author":"Zeilhofer","year":"2012","journal-title":"Physiol. Rev."},{"key":"10.1016\/j.neuron.2017.01.008_bib91","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/0006-8993(88)90146-1","article-title":"Nucleus cuneiformis and pain modulation: anatomy and behavioral pharmacology","volume":"453","author":"Zemlan","year":"1988","journal-title":"Brain Res."},{"key":"10.1016\/j.neuron.2017.01.008_bib92","doi-asserted-by":"crossref","first-page":"3782","DOI":"10.1172\/JCI81156","article-title":"Identifying local and descending inputs for primary sensory neurons","volume":"125","author":"Zhang","year":"2015","journal-title":"J.\u00a0Clin. Invest."},{"key":"10.1016\/j.neuron.2017.01.008_bib93","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1016\/j.neuron.2014.10.003","article-title":"Descending control of itch transmission by the serotonergic system via 5-HT1A-facilitated GRP-GRPR signaling","volume":"84","author":"Zhao","year":"2014","journal-title":"Neuron"},{"key":"10.1016\/j.neuron.2017.01.008_bib94","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.tins.2016.01.006","article-title":"Neural mechanisms underlying anxiety-chronic pain interactions","volume":"39","author":"Zhuo","year":"2016","journal-title":"Trends Neurosci."},{"key":"10.1016\/j.neuron.2017.01.008_bib95","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/0304-3959(90)91147-B","article-title":"Characterization of descending inhibition and facilitation from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat","volume":"42","author":"Zhuo","year":"1990","journal-title":"Pain"}],"container-title":["Neuron"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0896627317300107?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0896627317300107?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,6,14]],"date-time":"2025-06-14T19:41:09Z","timestamp":1749930069000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0896627317300107"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,2]]},"references-count":95,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2017,2]]}},"alternative-id":["S0896627317300107"],"URL":"https:\/\/doi.org\/10.1016\/j.neuron.2017.01.008","relation":{},"ISSN":["0896-6273"],"issn-type":[{"value":"0896-6273","type":"print"}],"subject":[],"published":{"date-parts":[[2017,2]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"A Brainstem-Spinal Cord Inhibitory Circuit for Mechanical Pain Modulation by GABA and Enkephalins","name":"articletitle","label":"Article Title"},{"value":"Neuron","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.neuron.2017.01.008","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2017 Elsevier Inc.","name":"copyright","label":"Copyright"}]}}