{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T09:03:04Z","timestamp":1789981384846,"version":"4.0.1"},"reference-count":48,"publisher":"Elsevier BV","issue":"1","license":[{"start":{"date-parts":[[2004,1,1]],"date-time":"2004-01-01T00:00:00Z","timestamp":1072915200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Brain Research"],"published-print":{"date-parts":[[2004,1]]},"DOI":"10.1016\/j.brainres.2003.10.050","type":"journal-article","created":{"date-parts":[[2003,12,12]],"date-time":"2003-12-12T14:45:28Z","timestamp":1071240328000},"page":"67-78","source":"Crossref","is-referenced-by-count":43,"title":["Activation of \u03bc-opioid receptors excites a population of locus coeruleus-spinal neurons through presynaptic disinhibition"],"prefix":"10.1016","volume":"997","author":[{"given":"Yu-Zhen","family":"Pan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"De-Pei","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shao-Rui","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hui-Lin","family":"Pan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.brainres.2003.10.050_BIB1","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/S0079-6123(08)63799-1","article-title":"Afferent regulation of locus coeruleus neurons: anatomy, physiology and pharmacology","volume":"88","author":"Aston-Jones","year":"1991","journal-title":"Prog. Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB2","doi-asserted-by":"crossref","first-page":"1331","DOI":"10.1177\/32.12.6150057","article-title":"Catecholaminergic and GABAergic anatomical relationship in the rat substantia nigra, locus coeruleus, and hypothalamic median eminence: immunocytochemical visualization of biosynthetic enzymes on serial semithin plastic-embedded sections","volume":"32","author":"Berod","year":"1984","journal-title":"J. Histochem. Cytochem."},{"key":"10.1016\/j.brainres.2003.10.050_BIB3","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1016\/0006-8993(77)90462-0","article-title":"Iontophoretic application of opiates to the locus coeruleus","volume":"122","author":"Bird","year":"1977","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB4","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1016\/0006-8993(90)90845-3","article-title":"Blockade of morphine analgesia by both pertussis and cholera toxins in the periaqueductal gray and locus coeruleus","volume":"529","author":"Bodnar","year":"1990","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB5","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1111\/j.1469-7793.1999.0551p.x","article-title":"Mechanism underlying increased neuronal activity in the rat ventrolateral periaqueductal grey by a mu-opioid","volume":"518","author":"Chiou","year":"1999","journal-title":"J. Physiol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB6","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/S0079-6123(08)63809-1","article-title":"Mechanisms of opioid actions on neurons of the locus coeruleus","volume":"88","author":"Christie","year":"1991","journal-title":"Prog. Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB7","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/0006-8993(92)90976-G","article-title":"Anatomical evidence for genetic differences in the innervation of the rat spinal cord by noradrenergic locus coeruleus neurons","volume":"591","author":"Clark","year":"1992","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB8","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/0006-8993(79)90661-9","article-title":"Locus coeruleus stimulation increases noradrenergic metabolite levels in rat spinal cord","volume":"166","author":"Crawley","year":"1979","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB9","doi-asserted-by":"crossref","first-page":"3162","DOI":"10.1523\/JNEUROSCI.12-08-03162.1992","article-title":"Robust enkephalin innervation of the locus coeruleus from the rostral medulla","volume":"12","author":"Drolet","year":"1992","journal-title":"J. Neurosci."},{"key":"10.1016\/j.brainres.2003.10.050_BIB10","doi-asserted-by":"crossref","first-page":"3644","DOI":"10.1523\/JNEUROSCI.08-10-03644.1988","article-title":"Activation of locus coeruleus from nucleus paragigantocellularis: a new excitatory amino acid pathway in brain","volume":"8","author":"Ennis","year":"1988","journal-title":"J. Neurosci."},{"key":"10.1016\/j.brainres.2003.10.050_BIB11","doi-asserted-by":"crossref","first-page":"2973","DOI":"10.1523\/JNEUROSCI.09-08-02973.1989","article-title":"GABA-mediated inhibition of locus coeruleus from the dorsomedial rostral medulla","volume":"9","author":"Ennis","year":"1989","journal-title":"J. Neurosci."},{"key":"10.1016\/j.brainres.2003.10.050_BIB12","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1016\/0361-9230(89)90022-1","article-title":"Potent inhibitory input to locus coeruleus from the nucleus prepositus hypoglossi","volume":"22","author":"Ennis","year":"1989","journal-title":"Brain Res. Bull."},{"key":"10.1016\/j.brainres.2003.10.050_BIB13","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1002\/cne.903060311","article-title":"Projections from the periaqueductal gray to the rostromedial pericoerulear region and nucleus locus coeruleus: anatomic and physiologic studies","volume":"306","author":"Ennis","year":"1991","journal-title":"J. Comp. Neurol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB14","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/0006-8993(92)90182-9","article-title":"Activation of locus coeruleus neurons by nucleus paragigantocellularis or noxious sensory stimulation is mediated by intracoerulear excitatory amino acid neurotransmission","volume":"598","author":"Ennis","year":"1992","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB15","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1002\/cne.902910406","article-title":"Demonstration of two separate descending noradrenergic pathways to the rat spinal cord: evidence for an intragriseal trajectory of locus coeruleus axons in the superficial layers of the dorsal horn","volume":"291","author":"Fritschy","year":"1990","journal-title":"J. Comp. Neurol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB16","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1016\/S0028-3908(01)00028-4","article-title":"Pharmacological modulation of SK3 channels","volume":"40","author":"Grunnet","year":"2001","journal-title":"Neuropharmacology"},{"key":"10.1016\/j.brainres.2003.10.050_BIB17","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/0006-8993(95)01430-6","article-title":"Long-latency responses of brain noradrenergic neurons to noxious stimuli are preferentially attenuated by intravenous morphine","volume":"714","author":"Hirata","year":"1996","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB18","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/0006-8993(87)90651-2","article-title":"Effect of spinal norepinephrine depletion on descending inhibition of the tail flick reflex from the locus coeruleus and lateral reticular nucleus in the rat","volume":"400","author":"Janss","year":"1987","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB19","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1016\/0006-8993(86)90844-9","article-title":"Characterization of coeruleospinal inhibition of the nociceptive tail-flick reflex in the rat: mediation by spinal alpha 2-adrenoceptors","volume":"364","author":"Jones","year":"1986","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB20","doi-asserted-by":"crossref","first-page":"1397","DOI":"10.1152\/jn.1986.56.5.1397","article-title":"Quantitative characterization of ceruleospinal inhibition of nociceptive transmission in the rat","volume":"56","author":"Jones","year":"1986","journal-title":"J. Neurophysiol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB21","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1152\/jn.1987.58.1.138","article-title":"Spinal pathways mediating tonic, coeruleospinal, and raphe-spinal descending inhibition in the rat","volume":"58","author":"Jones","year":"1987","journal-title":"J. Neurophysiol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB22","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/0006-8993(88)90373-3","article-title":"Inhibition of spinal nociceptive transmission from the midbrain, pons and medulla in the rat: activation of descending inhibition by morphine, glutamate and electrical stimulation","volume":"460","author":"Jones","year":"1988","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB23","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/0006-8993(94)90144-9","article-title":"Whole-cell patch-clamp recordings from visualized bulbospinal neurons in the brainstem slices","volume":"641","author":"Kangrga","year":"1994","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB24","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1111\/j.1469-7793.1999.0803p.x","article-title":"Actions of opioids on excitatory and inhibitory transmission in substantia gelatinosa of adult rat spinal cord","volume":"518","author":"Kohno","year":"1999","journal-title":"J. Physiol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB25","first-page":"49","article-title":"Reduced analgesic effects of morphine after bilateral lesions of the locus coeruleus in rats","volume":"30","author":"Kostowski","year":"1978","journal-title":"Pol. J. Pharmacol. Pharm."},{"key":"10.1016\/j.brainres.2003.10.050_BIB26","first-page":"R1005","article-title":"Potentiation of glutamatergic synaptic input to supraoptic neurons by presynaptic nicotinic receptors","volume":"281","author":"Li","year":"2001","journal-title":"Am. J. Physiol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB27","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1007\/BF00427132","article-title":"A pharmacologic study of analgesia produced by stimulation of the nucleus locus coeruleus","volume":"62","author":"Margalit","year":"1979","journal-title":"Psychopharmacology (Berl.)"},{"key":"10.1016\/j.brainres.2003.10.050_BIB28","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1002\/cne.902870109","article-title":"Effects of iontophoresis of noradrenaline and stimulation of the periaqueductal gray on single-unit activity in the rat superficial dorsal horn","volume":"287","author":"Millar","year":"1989","journal-title":"J. Comp. Neurol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB29","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1111\/j.1460-9568.1997.tb01361.x","article-title":"Electron microscopic distribution of mu opioid receptors on noradrenergic neurons of the locus coeruleus","volume":"9","author":"Moyse","year":"1997","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.brainres.2003.10.050_BIB30","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1113\/jphysiol.1985.sp015743","article-title":"On the potassium conductance increased by opioids in rat locus coeruleus neurones","volume":"364","author":"North","year":"1985","journal-title":"J. Physiol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB31","doi-asserted-by":"crossref","first-page":"2675","DOI":"10.1152\/jn.00298.2002","article-title":"Activation of delta-opioid receptors excites spinally projecting locus coeruleus neurons through inhibition of GABAergic Inputs","volume":"88","author":"Pan","year":"2002","journal-title":"J. Neurophysiol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB32","doi-asserted-by":"crossref","first-page":"1938","DOI":"10.1152\/jn.00575.2001","article-title":"Inhibition of glutamatergic synaptic input to spinal lamina IIo neurons by presynaptic alpha2-adrenergic receptors","volume":"87","author":"Pan","year":"2002","journal-title":"J. Neurophysiol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB33","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1016\/0306-4522(81)90169-X","article-title":"Demonstration of central gamma-aminobutyrate-containing nerve terminals by means of antibodies against glutamate decarboxylase","volume":"6","author":"Perez de la Mora","year":"1981","journal-title":"Neuroscience"},{"key":"10.1016\/j.brainres.2003.10.050_BIB34","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/0006-8993(85)90801-7","article-title":"Locus coeruleus unit activity in freely moving cats is increased following systemic morphine administration","volume":"344","author":"Rasmussen","year":"1985","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB35","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/0006-8993(77)90488-7","article-title":"Analgesia produced by electrical stimulation of catecholamine nuclei in the rat brain","volume":"123","author":"Segal","year":"1977","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB36","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/S0079-6123(08)63808-X","article-title":"GABAA and GABAB receptors and the ionic mechanisms mediating their effects on locus coeruleus neurons","volume":"88","author":"Shefner","year":"1991","journal-title":"Prog. Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB37","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1046\/j.0953-816x.2001.01638.x","article-title":"Patterns of colocalization of GABA, glutamate and glycine immunoreactivities in terminals that synapse on dendrites of noradrenergic neurons in rat locus coeruleus","volume":"14","author":"Somogyi","year":"2001","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.brainres.2003.10.050_BIB38","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/S0306-4522(00)00486-3","article-title":"Distribution of the messenger RNA for the small conductance calcium- activated potassium channel SK3 in the adult rat brain and correlation with immunoreactivity","volume":"102","author":"Tacconi","year":"2001","journal-title":"Neuroscience"},{"key":"10.1016\/j.brainres.2003.10.050_BIB39","first-page":"1178","article-title":"Morphine effects on locus ceruleus neurons are dependent on the state of arousal and availability of external stimuli: studies in anesthetized and unanesthetized rats","volume":"244","author":"Valentino","year":"1988","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"10.1016\/j.brainres.2003.10.050_BIB40","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/S0006-8993(96)01194-8","article-title":"Electron microscopic evidence for coexistence of leucine5-enkephalin and gamma-aminobutyric acid in a subpopulation of axon terminals in the rat locus coeruleus region","volume":"746","author":"van Bockstaele","year":"1997","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB41","doi-asserted-by":"crossref","first-page":"5037","DOI":"10.1523\/JNEUROSCI.16-16-05037.1996","article-title":"Ultrastructural evidence for prominent distribution of the mu-opioid receptor at extrasynaptic sites on noradrenergic dendrites in the rat nucleus locus coeruleus","volume":"16","author":"van Bockstaele","year":"1996","journal-title":"J. Neurosci."},{"key":"10.1016\/j.brainres.2003.10.050_BIB42","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1002\/(SICI)1096-9861(19961202)376:1<65::AID-CNE4>3.0.CO;2-M","article-title":"Mu-opioid receptor is located on the plasma membrane of dendrites that receive asymmetric synapses from axon terminals containing leucine\u2013enkephalin in the rat nucleus locus coeruleus","volume":"376","author":"van Bockstaele","year":"1996","journal-title":"J. Comp. Neurol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB43","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1002\/(SICI)1096-9861(20000131)417:1<103::AID-CNE8>3.0.CO;2-L","article-title":"Evidence for coexistence of enkephalin and glutamate in axon terminals and cellular sites for functional interactions of their receptors in the rat locus coeruleus","volume":"417","author":"van Bockstaele","year":"2000","journal-title":"J. Comp. Neurol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB44","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1113\/jphysiol.1997.sp021872","article-title":"Presynaptic inhibitory action of opioids on synaptic transmission in the rat periaqueductal grey in vitro","volume":"498","author":"Vaughan","year":"1997","journal-title":"J. Physiol."},{"key":"10.1016\/j.brainres.2003.10.050_BIB45","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1038\/37610","article-title":"How opioids inhibit GABA-mediated neurotransmission","volume":"390","author":"Vaughan","year":"1997","journal-title":"Nature"},{"key":"10.1016\/j.brainres.2003.10.050_BIB46","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/0006-8993(93)90571-4","article-title":"The function of noradrenergic neurons in mediating antinociception induced by electrical stimulation of the locus coeruleus in two different sources of Sprague\u2013Dawley rats","volume":"626","author":"West","year":"1993","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB47","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/0006-8993(83)91196-4","article-title":"Noradrenergic projections to the spinal cord of the rat","volume":"263","author":"Westlund","year":"1983","journal-title":"Brain Res."},{"key":"10.1016\/j.brainres.2003.10.050_BIB48","doi-asserted-by":"crossref","first-page":"RC179","DOI":"10.1523\/JNEUROSCI.21-21-j0003.2001","article-title":"Morphine induces synchronous oscillatory discharges in the rat locus coeruleus","volume":"21","author":"Zhu","year":"2001","journal-title":"J. Neurosci."}],"container-title":["Brain Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0006899303039647?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0006899303039647?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2020,3,28]],"date-time":"2020-03-28T01:18:25Z","timestamp":1585358305000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0006899303039647"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2004,1]]},"references-count":48,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2004,1]]}},"alternative-id":["S0006899303039647"],"URL":"https:\/\/doi.org\/10.1016\/j.brainres.2003.10.050","relation":{},"ISSN":["0006-8993"],"issn-type":[{"value":"0006-8993","type":"print"}],"subject":[],"published":{"date-parts":[[2004,1]]}}}