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Neurochemically distinct circuitry regulates locus coeruleus activity during female social stress depending on coping style

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Abstract

Stress-related psychiatric diseases are nearly twice as prevalent in women compared to men. We recently showed in male rats that the resident–intruder model of social stress differentially engages stress-related circuitry that regulates norepinephrine-containing neurons of the locus coeruleus (LC) depending on coping strategy as determined by the latency to assume a defeat posture. Here, we determined whether this social stress had similar effects in female rats. LC afferents were retrogradely labeled with Fluorogold (FG) and rats had one or five daily exposures to an aggressive resident. Sections through the nucleus paragigantocellularis (PGi), a source of enkephalin (ENK) afferents to the LC, and central nucleus of the amygdala (CeA), a source of corticotropin-releasing factor (CRF) afferents to the LC, were processed for immunocytochemical detection of c-fos, a marker of neuronal activity, FG and ENK or CRF. Like male rats, female rats defeated with a relatively short latency (SL) in response to a single resident–intruder exposure and showed significant c-fos activation of LC neurons, PGi-ENK LC afferents, and CeA-CRF-LC afferents. With repeated exposure, some rats exhibited a long latency to defeat (LL). LC neurons and CeA-CRF-LC afferents were activated in SL rats compared to control and LL, whereas PGi-ENK LC afferents were not. Conversely, in LL rats, PGi-ENK LC and CeA-CRF-LC afferents were activated compared to controls but not LC neurons. CRF type 1 receptor (CRF1) and µ-opioid receptor (MOR) expression levels in LC were decreased in LL rats. Finally, electron microscopy showed a relative increase in MOR on the plasma membrane of LL rats and a relative increase in CRF1 on the plasma membrane of SL rats. Together, these results suggest that as is the case for males, social stress engages divergent circuitry to regulate the LC in female rats depending on coping strategy, with a bias towards CRF influence in more subordinate rats and opioid influence in less subordinate rats.

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References

  • Andrezik JA, Chan-Palay V, Palay SL (1981) The nucleus paragigantocellularis lateralis in the rat. Conformation and cytology. Anat Embryol (Berl) 161:355–371

    Article  CAS  Google Scholar 

  • Avgustinovich DF, Kovalenko IL, Kudryavtseva NN (2005) A model of anxious depression: persistence of behavioral pathology. Neurosci Behav Physiol 35:917–924

    Article  CAS  PubMed  Google Scholar 

  • Bangasser DA, Valentino RJ (2012) Sex differences in molecular and cellular substrates of stress. Cell Mol Neurobiol 32:709–723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bangasser DA, Curtis A, Reyes BA, Bethea TT, Parastatidis I, Ischiropoulos H, Van Bockstaele EJ, Valentino RJ (2010) Sex differences in corticotropin-releasing factor receptor signaling and trafficking: potential role in female vulnerability to stress-related psychopathology. Mol Psychiatry 15(877):896–904

    Article  CAS  Google Scholar 

  • Barr J, Van Bockstaele EJ (2005) Vesicular glutamate transporter-1 colocalizes with endogenous opioid peptides in axon terminals of the rat locus coeruleus. Anat Rec 284:466–474

    Article  CAS  Google Scholar 

  • Berridge CW, Waterhouse BD (2003) The locus-coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Rev 42:33–84

    Article  PubMed  Google Scholar 

  • Bissette G, Klimek V, Pan J, Stockmeier C, Ordway G (2003) Elevated concentrations of CRF in the locus coeruleus of depressed subjects. Neuropsychopharmacology 28:1328–1335

    Article  CAS  PubMed  Google Scholar 

  • Breen KM, Davis TL, Doro LC, Nett TM, Oakley AE, Padmanabhan V, Rispoli LA, Wagenmaker ER, Karsch FJ (2008) Insight into the neuroendocrine site and cellular mechanism by which cortisol suppresses pituitary responsiveness to gonadotropin-releasing hormone. Endocrinology 149:767–773

    Article  CAS  PubMed  Google Scholar 

  • Chaijale NN, Curtis AL, Wood SK, Zhang XY, Bhatnagar S, Reyes BA, Van Bockstaele EJ, Valentino RJ (2013) Social stress engages opioid regulation of locus coeruleus norepinephrine neurons and induces a state of cellular and physical opiate dependence. Neuropsychopharmacology 38:1833–1843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen RJ, Kelly G, Sengupta A, Heydendael W, Nicholas B, Beltrami S, Luz S, Peixoto L, Abel T, Bhatnagar S (2015) MicroRNAs as biomarkers of resilience or vulnerability to stress. Neuroscience 305:36–48

    Article  CAS  PubMed  Google Scholar 

  • Cheng PY, Moriwaki A, Wang JB, Uhl GR, Pickel VM (1996) Ultrastructural localization of mu-opioid receptors in the superficial layers of the rat cervical spinal cord: extrasynaptic localization and proximity to Leu5-enkephalin. Brain Res 731:141–154

    Article  CAS  PubMed  Google Scholar 

  • Curtis AL, Lechner SM, Pavcovich LA, Valentino RJ (1997) Activation of the locus coeruleus noradrenergic system by intracoerulear microinfusion of corticotropin-releasing factor: effects on discharge rate, cortical norepinephrine levels and cortical electroencephalographic activity. J Pharmacol Exp Ther 281:163–172

    CAS  PubMed  Google Scholar 

  • Curtis AL, Bello NT, Valentino RJ (2001) Evidence for functional release of endogenous opioids in the locus ceruleus during stress termination. J Neurosci 21:RC152

    Article  CAS  PubMed  Google Scholar 

  • Curtis AL, Leiser SC, Snyder K, Valentino RJ (2012) Predator stress engages corticotropin-releasing factor and opioid systems to alter the operating mode of locus coeruleus norepinephrine neurons. Neuropharmacology 62:1737–1745

    Article  CAS  PubMed  Google Scholar 

  • Dai X, Noga BR, Douglas JR, Jordan LM (2005) Localization of spinal neurons activated during locomotion using the c-fos immunohistochemical method. J Neurophysiol 93:3442–3452

    Article  CAS  PubMed  Google Scholar 

  • de Kloet ER, Joels M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463–475

    Article  CAS  PubMed  Google Scholar 

  • Drolet G, Van Bockstaele EJ, Aston-Jones G (1992) Robust enkephalin innervation of the locus coeruleus from the rostral medulla. J Neurosci 12:3162–3174

    Article  CAS  PubMed  Google Scholar 

  • Ehnert K, Moberg GP (1991) Disruption of estrous behavior in ewes by dexamethasone or management-related stress. J Animal Science 69:2988–2994

    Article  CAS  Google Scholar 

  • Enman NM, Reyes BAS, Shi Y, Valentino RJ, Van Bockstaele EJ (2018) Sex differences in morphine-induced trafficking of mu-opioid and corticotropin-releasing factor receptors in locus coeruleus neurons. Brain Res. https://doi.org/10.1016/j.brainres.2018.11.001

    Article  PubMed  Google Scholar 

  • Flannelly KJ, Flannelly L (1987) Time course of postpartum aggression in rats (Rattus norvegicus). J Comp Psychol 101:101–103

    Article  Google Scholar 

  • Ghosal K, Naples SP, Rabe AR, Killian KA (2010) Agonistic behavior and electrical stimulation of the antennae induces Fos-like protein expression in the male cricket brain. Arch Insect Biochem Physiol 74:38–51

    Article  CAS  PubMed  Google Scholar 

  • Gold PW, Chrousos GP (2002) Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Mol Psychiatry 7:254–275

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez AS, Rodriguez Echandia EL, Cabrera R, Foscolo MR (1994) Neonatal chronic stress induces subsensitivity to chronic stress in adult rats: II. Effects on estrous cycle in females. Physiol Behav 56:591–595

    Article  CAS  PubMed  Google Scholar 

  • Gorenstein C, Bundman MC, Lew PJ, Olds JL, Ribak CE (1985) Dendritic transport. I. Colchicine stimulates the transport of lysosomal enzymes from cell bodies to dendrites. J Neurosci 5:2009–2017

    Article  CAS  PubMed  Google Scholar 

  • Grillon C, Southwick SM, Charney DS (1996) The psychobiological basis of posttraumatic stress disorder. Mol Psychiatry 1:278–297

    CAS  PubMed  Google Scholar 

  • Guajardo HM, Snyder K, Ho A, Valentino RJ (2017) Sex differences in mu-opioid receptor regulation of the rat locus coeruleus and their cognitive consequences. Neuropsychopharmacology 42:1295–1304

    Article  CAS  PubMed  Google Scholar 

  • Jia Y, Yao H, Zhou J, Chen L, Zeng Q, Yuan H, Shi L, Nan X, Wang Y, Yue W, Pei X (2011) Role of epimorphin in bile duct formation of rat liver epithelial stem-like cells: involvement of small G protein RhoA and C/EBPbeta. J Cellular Physiol 226:2807–2816

    Article  CAS  Google Scholar 

  • Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MA, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935

    Article  CAS  PubMed  Google Scholar 

  • Kravets JL, Reyes BA, Unterwald EM, Van Bockstaele EJ (2015) Direct targeting of peptidergic amygdalar neurons by noradrenergic afferents: linking stress-integrative circuitry. Brain Struct Funct 220:541–558

    Article  CAS  PubMed  Google Scholar 

  • Leranth C, Pickel VM (1989) Electron microscopic preembedding double-labeling methods. In: Heimer L, Zaborszky L (eds) Neuroanatomical tracing methods, vol 2, 1st edn. Plenum Press, New York, pp 129–172

    Chapter  Google Scholar 

  • Li XF, Hu MH, Li SY et al (2014) Overexpression of corticotropin releasing factor in the central nucleus of the amygdala advances puberty and disrupts reproductive cycles in female rats. Endocrinology 155:3934–3944

    Article  CAS  PubMed  Google Scholar 

  • Marchlewska-Koj A, Pochron E, Galewicz-Sojecka A, Galas J (1994) Suppression of estrus in female mice by the presence of conspecifics or by foot shock. Physiol Behav 55:317–321

    Article  CAS  PubMed  Google Scholar 

  • Matsuzaki H, Izumi T, Horinouchi T, Boku S, Inoue T, Yamaguchi T, Yoshida T, Matsumoto M, Togashi H, Miwa S, Koyama T, Yoshioka M (2011) Juvenile stress attenuates the dorsal hippocampal postsynaptic 5-HT1A receptor function in adult rats. Psychopharmacology (Berl) 214:329–337

    Article  CAS  Google Scholar 

  • McEwen BS (1998) Stress, adaptation, and disease. Allostasis and allostatic load. Ann N Y Acad Sci 840:33–44

    Article  CAS  PubMed  Google Scholar 

  • Melia KR, Duman RS (1991) Involvement of corticotropin-releasing factor in chronic stress regulation of the brain noradrenergic system. Proc Natl Acad Sci USA 88:8382–8386

    Article  CAS  PubMed  Google Scholar 

  • Miczek KA (1979) A new test for aggression in rats without aversive stimulation: differential effects of d-amphetamine and cocaine. Psychopharmacology 60:253–259

    Article  CAS  Google Scholar 

  • Miczek KA, Covington HE III, Nikulina EM Jr, Hammer RP (2004) Aggression and defeat: persistent effects on cocaine self-administration and gene expression in peptidergic and aminergic mesocorticolimbic circuits. Neurosci Biobehav Rev 27:787–802

    Article  CAS  PubMed  Google Scholar 

  • Miczek KA, Thompson ML, Shuster L (1982) Opioid-like analgesia in defeated mice. Science 215:1520–1522

    Article  CAS  PubMed  Google Scholar 

  • Milner TA, Okada J, Pickel VM (1995) Monosynaptic input from Leu5-enkephalin-immunoreactive terminals to vagal motor neurons in the nucleus ambiguus: comparison with the dorsal motor nucleus of the vagus. J Comp Neurol 353:391–406

    Article  CAS  PubMed  Google Scholar 

  • Monti-Graziadei AG, Berkley KJ (1991) Effects of colchicine on retrogradely-transported WGA-HRP. Brain Res 565:162–166

    Article  CAS  PubMed  Google Scholar 

  • Nikulina EM, Hammer RP Jr, Miczek KA, Kream RM (1999) Social defeat stress increases expression of mu-opioid receptor mRNA in rat ventral tegmental area. Neuroreport 10:3015–3019

    Article  CAS  PubMed  Google Scholar 

  • Nikulina EM, Arrillaga-Romany I, Miczek KA, Hammer RP Jr (2008) Long-lasting alteration in mesocorticolimbic structures after repeated social defeat stress in rats: time course of mu-opioid receptor mRNA and FosB/DeltaFosB immunoreactivity. Eur J Neurosci 27:2272–2284

    Article  PubMed  PubMed Central  Google Scholar 

  • Noga BR, Johnson DM, Riesgo MI, Pinzon A (2011) Locomotor-activated neurons of the cat. II. Noradrenergic innervation and colocalization with NEalpha 1a or NEalpha 2b receptors in the thoraco-lumbar spinal cord. J Neurophysiol 105:1835–1849

    Article  PubMed  PubMed Central  Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, North Ryde

    Google Scholar 

  • Pearson-Leary J, Eacret D, Chen R, Takano H, Nicholas B, Bhatnagar S (2017) Inflammation and vascular remodeling in the ventral hippocampus contributes to vulnerability to stress. Transl Psychiatry 7:e1160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng J, Sarkar S, Chang SL (2012) Opioid receptor expression in human brain and peripheral tissues using absolute quantitative real-time RT-PCR. Drug Alcohol Depend 124:223–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pierce BN, Hemsworth PH, Rivalland ET, Wagenmaker ER, Morrissey AD, Papargiris MM, Clarke IJ, Karsch FJ, Turner AI, Tilbrook AJ (2008) Psychosocial stress suppresses attractivity, proceptivity and pulsatile LH secretion in the ewe. Horm Behav 54:424–434

    Article  CAS  PubMed  Google Scholar 

  • Pietrzak RH, Gallezot JD, Ding YS, Henry S, Potenza MN, Southwick SM, Krystal JH, Carson RE, Neumeister A (2013) Association of posttraumatic stress disorder with reduced in vivo norepinephrine transporter availability in the locus coeruleus. JAMA Psychiatry 70:1199–1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Por E, Byun HJ, Lee EJ, Lim JH, Jung SY, Park I, Kim YM, Jeoung DI, Lee H (2010) The cancer/testis antigen CAGE with oncogenic potential stimulates cell proliferation by up-regulating cyclins D1 and E in an AP-1- and E2F-dependent manner. J Biol Chem 285:14475–14485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Retson TA, Hoek JB, Sterling RC, Van Bockstaele EJ (2015) Amygdalar neuronal plasticity and the interactions of alcohol, sex, and stress. Brain Struct Funct 220:3211–3232

    Article  CAS  PubMed  Google Scholar 

  • Reyes BA, Valentino RJ, Xu G, Van Bockstaele EJ (2005) Hypothalamic projections to locus coeruleus neurons in rat brain. Eur J Neurosci 22:93–106

    Article  PubMed  Google Scholar 

  • Reyes BAS, Fox K, Valentino RJ, Van Bockstaele EJ (2006) Agonist-induced internalization of corticotropin-releasing factor receptors in noradrenergic neurons of the rat locus coeruleus. Eur J Neurosci 23:2991–2998

    Article  PubMed  Google Scholar 

  • Reyes BA, Valentino RJ, Van Bockstaele EJ (2008) Stress-induced intracellular trafficking of corticotropin-releasing factor receptors in rat locus coeruleus neurons. Endocrinology 149:122–130

    Article  CAS  PubMed  Google Scholar 

  • Reyes BA, Carvalho AF, Vakharia K, Van Bockstaele EJ (2011) Amygdalar peptidergic circuits regulating noradrenergic locus coeruleus neurons: linking limbic and arousal centers. Exp Neurol 230:96–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reyes BA, Zitnik G, Foster C, Van Bockstaele EJ, Valentino RJ (2015) Social stress engages neurochemically-distinct afferents to the rat locus coeruleus depending on coping strategy. eNeuro. https://doi.org/10.1523/ENEURO.0042-15.2015. (eCollection 2015)

    Article  PubMed  PubMed Central  Google Scholar 

  • Rite I, Venero JL, Tomas-Camardiel M, Machado A, Cano J (2003) Expression of BDNF mRNA in substantia nigra is dependent on target integrity and independent of neuronal activation. J Neurochem 87:709–721

    Article  CAS  PubMed  Google Scholar 

  • Rygula R, Abumaria N, Flugge G, Fuchs E, Ruther E, Havemann-Reinecke U (2005) Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav Brain Res 162:127–134

    Article  PubMed  Google Scholar 

  • Stoeber M, Jullie D, Lobingier BT, Laeremans T, Steyaert J, Schiller PW, Manglik A, von Zastrow M (2018) A genetically encoded biosensor reveals location bias of opioid drug action. Neuron 98:963–976 e965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Surratt CK, Johnson PS, Moriwaki A, Seidleck BK, Blaschak CJ, Wang JB, Uhl GR (1994) -mu opiate receptor. Charged transmembrane domain amino acids are critical for agonist recognition and intrinsic activity. J Biol Chem 269:20548–20553

    CAS  PubMed  Google Scholar 

  • Sutherland JE, Burian LC, Covault J, Conti LH (2010) The effect of restraint stress on prepulse inhibition and on corticotropin-releasing factor (CRF) and CRF receptor gene expression in Wistar–Kyoto and Brown Norway rats. Pharmacol Biochem Behav 97:227–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teskey GC, Kavaliers M, Hirst M (1984) Social conflict activates opioid analgesic and ingestive behaviors in male mice. Life Sci 35:303–315

    Article  CAS  PubMed  Google Scholar 

  • Tjoumakaris SI, Rudoy C, Peoples J, Valentino RJ, Van Bockstaele EJ (2003) Cellular interactions between axon terminals containing endogenous opioid peptides or corticotropin-releasing factor in the rat locus coeruleus and surrounding dorsal pontine tegmentum. J Comp Neurol 466:445–456

    Article  CAS  PubMed  Google Scholar 

  • Valentino RJ, Van Bockstaele E (2008) Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur J Pharmacol 583:194–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Bockstaele EJ, Branchereau P, Pickel VM (1995) Morphologically heterogeneous met-enkephalin terminals form synapses with tyrosine hydroxylase-containing dendrites in the rat nucleus locus coeruleus. J Comp Neurol 363:423–438

    Article  PubMed  Google Scholar 

  • Van Bockstaele EJ, Colago EEO, Cheng P, Moriwaki A, Uhl GR, Pickel VM (1996a) Ultrastructural evidence for prominent distribution of the mu-opioid receptor at extrasynaptic sites on noradrenergic dendrites in the rat nucleus locus coeruleus. J Neurosci 16:5037–5048

    Article  PubMed  Google Scholar 

  • Van Bockstaele EJ, Colago EEO, Moriwaki A, Uhl GR (1996b) Mu-opioid receptor is located on the plasma membrane of dendrites that receive asymmetric synapses from axon terminals containing leucine-enkephalin in the rat nucleus locus coeruleus. J Comp Neurol 376:65–74

    Article  PubMed  Google Scholar 

  • Van Bockstaele EJ, Colago EEO, Valentino RJ (1996c) Corticotropin-releasing factor-containing axon terminals synapse onto catecholamine dendrites and may presynaptically modulate other afferents int he rostral pole of the nucleus locus coeruleus in the rat brain. J Comp Neurol 364:523–534

    Article  PubMed  Google Scholar 

  • Van Bockstaele EJ, Colago EE, Valentino RJ (1998) Amygdaloid corticotropin-releasing factor targets locus coeruleus dendrites: substrate for the co-ordination of emotional and cognitive limbs of the stress response. J Neuroendocrinol 10:743–757

    Article  PubMed  Google Scholar 

  • Ventura C, Bastagli L, Bernardi P, Caldarera CM, Guarnieri C (1989) Opioid receptors in rat cardiac sarcolemma: effect of phenylephrine and isoproterenol. Biochem Biophys Acta 987:69–74

    Article  CAS  PubMed  Google Scholar 

  • Ver Hoeve ES, Kelly G, Luz S, Ghanshani S, Bhatnagar S (2013) Short-term and long-term effects of repeated social defeat during adolescence or adulthood in female rats. Neuroscience 249:63–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vicario M, Alonso C, Guilarte M, Serra J, Martinez C, Gonzalez-Castro AM, Lobo B, Antolin M, Andreu AL, Garcia-Arumi E, Casellas M, Saperas E, Malagelada JR, Azpiroz F, Santos J (2012) Chronic psychosocial stress induces reversible mitochondrial damage and corticotropin-releasing factor receptor type-1 upregulation in the rat intestine and IBS-like gut dysfunction. Psychoneuroendocrinology 37:65–77

    Article  CAS  PubMed  Google Scholar 

  • Wong ML, Kling MA, Munson PJ, Listwak S, Licinio J, Prolo P, Karp B, McCutcheon IE, Geracioti TD Jr, DeBellis MD, Rice KC, Goldstein DS, Veldhuis JD, Chrousos GP, Oldfield EH, McCann SM, Gold PW (2000) Pronounced and sustained central hypernoradrenergic function in major depression with melancholic features: relation to hypercortisolism and corticotropin-releasing hormone. Proc Natl Acad Sci USA 97:325–330

    Article  CAS  PubMed  Google Scholar 

  • Wood SK, Baez MA, Bhatnagar S, Valentino RJ (2009) Social stress-induced bladder dysfunction: potential role of corticotropin-releasing factor. Am J Physiol Regul Integr Comp Physiol 296:R1671–R1678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wood SK, Walker HE, Valentino RJ, Bhatnagar S (2010) Individual differences in reactivity to social stress predict susceptibility and resilience to a depressive phenotype: role of corticotropin-releasing factor. Endocrinology 151:1795–1805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wood SK, McFadden KV, Grigoriadis D, Bhatnagar S, Valentino RJ (2012) Depressive and cardiovascular disease comorbidity in a rat model of social stress: a putative role for corticotropin-releasing factor. Psychopharmacology 222:325–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wood SK, Wood CS, Lombard CM, Lee CS, Zhang XY, Finnell JE, Valentino RJ (2015) Inflammatory factors mediate vulnerability to a social stress-induced depressive-like phenotype in passive coping rats. Biol Psychiatry 78:38–48

    Article  CAS  PubMed  Google Scholar 

  • Xu G-P, Van Bockstaele EJ, Reyes BA, Bethea T, Valentino RJ (2004) Chronic morphine sensitizes the brain norepinephrine system to corticotropin-releasing factor and stress. J Neurosci 24:8193–8197

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Pharmacology and Physiology, College of Medicine, Drexel University, 245 S. 15th Street, Philadelphia, PA, 19102, USA

    Beverly A. S. Reyes, Elsa C. Dufourt & Elisabeth J. Van Bockstaele

  2. Department of Anesthesiology and Critical Care Medicine, Children’s Hospital of Philadelphia, Philadelphia, PA, 19104, USA

    Xiao-Yan Zhang, Seema Bhatnagar & Rita J. Valentino

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  1. Beverly A. S. Reyes
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Reyes, B.A.S., Zhang, XY., Dufourt, E.C. et al. Neurochemically distinct circuitry regulates locus coeruleus activity during female social stress depending on coping style. Brain Struct Funct 224, 1429–1446 (2019). https://doi.org/10.1007/s00429-019-01837-5

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