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Archival Report| Volume 69, ISSUE 11, P1083-1090, June 01, 2011

β-Adrenergic Receptors Enhance Excitatory Transmission in the Bed Nucleus of the Stria Terminalis Through a Corticotrophin-Releasing Factor Receptor–Dependent and Cocaine-Regulated Mechanism

  • William P. Nobis
    Affiliations
    Neuroscience Graduate Program, Center Molecular Neuroscience, Vanderbilt University School of Medicine, Nashville, Tennessee
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  • Thomas L. Kash
    Affiliations
    Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, Tennessee
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  • Yuval Silberman
    Affiliations
    Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, Tennessee
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  • Danny G. Winder
    Correspondence
    Address correspondence to Danny Winder, Ph.D., Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, TN 37232
    Affiliations
    Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, Tennessee

    Kennedy Center for Research on Human Development, Vanderbilt University School of Medicine, Nashville, Tennessee
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Published:February 22, 2011DOI:https://doi.org/10.1016/j.biopsych.2010.12.030

      Background

      Evidence suggests that the noradrenergic and corticotrophin-releasing factor (CRF) systems play critical roles in relapse and stress-related behaviors. In particular, behavioral studies point to a serial signaling process initiated by β-adrenergic receptors that requires CRF receptor (CRFR)-dependent signaling in the bed nucleus of the stria terminalis (BNST) to produce stress-induced relapse to cocaine seeking.

      Methods

      We used whole cell patch clamp recordings from acutely prepared mouse brain slices to examine the actions of β-adrenergic receptors and CRFR1 on excitatory transmission in BNST. We examined the effects of agonists of these receptors in slices prepared from naive, sham, and cocaine-conditioned mice.

      Results

      β1-adrenergic receptor activation within the BNST produces an enhancement of excitatory synaptic transmission that requires CRFR1-dependent signaling. We show that chronic cocaine administration transiently disrupts β1-adrenergic- and CRFR1-dependent enhancement of glutamatergic transmission, that this disruption wanes with time, and that it can be reintroduced with a cocaine challenge.

      Conclusions

      In total, these studies identify a circuit mechanism within the BNST that may play an important role in CRF- and norepinephrine-regulated behaviors.

      Key Words

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      References

        • Koob G.F.
        A role for brain stress systems in addiction.
        Neuron. 2008; 59: 11-34
        • Piazza P.V.
        • Le Moal M.
        The role of stress in drug self-administration.
        Trends Pharmacol Sci. 1998; 19: 67-74
        • Sinha R.
        Chronic stress, drug use, and vulnerability to addiction.
        Ann N Y Acad Sci. 2008; 1141: 105-130
        • Tsigos C.
        • Chrousos G.P.
        Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress.
        J Psychosom Res. 2002; 53: 865-871
        • Koob G.F.
        Corticotropin-releasing factor, norepinephrine, and stress.
        Biol Psychiatry. 1999; 46: 1167-1180
        • Goeders N.E.
        • Guerin G.F.
        Effects of the CRH receptor antagonist CP-154,526 on intravenous cocaine self-administration in rats.
        Neuropsychopharmacology. 2000; 23: 577-586
        • Piazza P.V.
        • Le Moal M.L.
        Pathophysiological basis of vulnerability to drug abuse: Role of an interaction between stress, glucocorticoids, and dopaminergic neurons.
        Annu Rev Pharmacol Toxicol. 1996; 36: 359-378
        • Delfs J.M.
        • Zhu Y.
        • Druhan J.P.
        • Aston-Jones G.
        Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion.
        Nature. 2000; 403: 430-434
        • Heinrichs S.C.
        • Menzaghi F.
        • Schulteis G.
        • Koob G.F.
        • Stinus L.
        Suppression of corticotropin-releasing factor in the amygdala attenuates aversive consequences of morphine withdrawal.
        Behav Pharmacol. 1995; 6: 74-80
        • Menzaghi F.
        • Rassnick S.
        • Heinrichs S.
        • Baldwin H.
        • Pich E.M.
        • Weiss F.
        • Koob G.F.
        The role of corticotropin-releasing factor in the anxiogenic effects of ethanol withdrawal.
        Ann N Y Acad Sci. 1994; 739: 176-184
        • Rodriguez de Fonseca F.
        • Carrera M.R.
        • Navarro M.
        • Koob G.F.
        • Weiss F.
        Activation of corticotropin-releasing factor in the limbic system during cannabinoid withdrawal.
        Science. 1997; 276: 2050-2054
        • Sarnyai Z.
        • Biro E.
        • Gardi J.
        • Vecsernyes M.
        • Julesz J.
        • Telegdy G.
        Brain corticotropin-releasing factor mediates “anxiety-like” behavior induced by cocaine withdrawal in rats.
        Brain Res. 1995; 675: 89-97
        • Erb S.
        • Hitchcott P.K.
        • Rajabi H.
        • Mueller D.
        • Shaham Y.
        • Stewart J.
        Alpha-2 adrenergic receptor agonists block stress-induced reinstatement of cocaine seeking.
        Neuropsychopharmacology. 2000; 23: 138-150
        • Erb S.
        • Shaham Y.
        • Stewart J.
        The role of corticotropin-releasing factor and corticosterone in stress- and cocaine-induced relapse to cocaine seeking in rats.
        J Neurosci. 1998; 18: 5529-5536
        • Le A.D.
        • Harding S.
        • Juzytsch W.
        • Watchus J.
        • Shalev U.
        • Shaham Y.
        The role of corticotrophin-releasing factor in stress-induced relapse to alcohol-seeking behavior in rats.
        Psychopharmacology (Berl). 2000; 150: 317-324
        • Shaham Y.
        • Funk D.
        • Erb S.
        • Brown T.J.
        • Walker C.D.
        • Stewart J.
        Corticotropin-releasing factor, but not corticosterone, is involved in stress-induced relapse to heroin-seeking in rats.
        J Neurosci. 1997; 17: 2605-2614
        • Shaham Y.
        • Highfield D.
        • Delfs J.
        • Leung S.
        • Stewart J.
        Clonidine blocks stress-induced reinstatement of heroin seeking in rats: An effect independent of locus coeruleus noradrenergic neurons.
        Eur J Neurosci. 2000; 12: 292-302
        • Leri F.
        • Flores J.
        • Rodaros D.
        • Stewart J.
        Blockade of stress-induced but not cocaine-induced reinstatement by infusion of noradrenergic antagonists into the bed nucleus of the stria terminalis or the central nucleus of the amygdala.
        J Neurosci. 2002; 22: 5713-5718
        • Brown Z.
        • Tribe E.
        • D'Souza N.
        • Erb S.
        Interaction between noradrenaline and corticotrophin-releasing factor in the reinstatement of cocaine seeking in the rat.
        Psychopharmacology. 2009; 203: 121-130
        • Aston-Jones G.
        • Delfs J.M.
        • Druhan J.
        • Zhu Y.
        The bed nucleus of the stria terminalis.
        Ann N Y Acad Sci. 1999; 877: 486-498
        • Harris G.C.
        • Aston-Jones G.
        Activation in extended amygdala corresponds to altered hedonic processing during protracted morphine withdrawal.
        Behav Brain Res. 2007; 176: 251-258
        • Erb S.
        • Stewart J.
        A role for the bed nucleus of the stria terminalis, but not the amygdala, in the effects of corticotropin-releasing factor on stress-induced reinstatement of cocaine seeking.
        J Neurosci. 1999; 19 (35RC–35RC)
        • Buffalari D.M.
        • See R.E.
        Inactivation of the bed nucleus of the stria terminalis in an animal model of relapse: Effects on conditioned cue-induced reinstatement and its enhancement by yohimbine.
        Psychopharmacology (Berl). 2011; 213: 19-27
        • Egli R.E.
        • Kash T.L.
        • Choo K.
        • Savchenko V.
        • Matthews R.T.
        • Blakely R.D.
        • et al.
        Norepinephrine modulates glutamatergic transmission in the bed nucleus of the stria terminalis.
        Neuropsychopharmacology. 2004; 30: 657-668
        • Kash T.L.
        • Nobis W.P.
        • Matthews R.T.
        • Winder D.G.
        Dopamine enhances fast excitatory synaptic transmission in the extended amygdala by a CRF-R1-dependent process.
        J Neurosci. 2008; 28: 13856-13865
        • Kash T.L.
        • Winder D.G.
        Neuropeptide Y and corticotropin-releasing factor bi-directionally modulate inhibitory synaptic transmission in the bed nucleus of the stria terminalis.
        Neuropharmacology. 2006; 51: 1013-1022
        • McElligott Z.A.
        • Winder D.G.
        Alpha1-adrenergic receptor-induced heterosynaptic long-term depression in the bed nucleus of the stria terminalis is disrupted in mouse models of affective disorders.
        Neuropsychopharmacology. 2008; 33: 2313-2323
        • McElligott Z.A.
        • Klug J.R.
        • Nobis W.P.
        • Patel S.
        • Grueter B.A.
        • Kash T.L.
        • Winder D.G.
        Distinct forms of Gq-receptor-dependent plasticity of excitatory transmission in the BNST are differentially affected by stress.
        Proc Natl Acad Sci U S A. 2010; 107: 2271-2276
        • Egli R.E.
        • Kash T.L.
        • Choo K.
        • Savchenko V.
        • Matthews R.T.
        • Blakely R.D.
        • Winder D.G.
        Norepinephrine modulates glutamatergic transmission in the bed nucleus of the stria terminalis.
        Neuropsychopharmacology. 2005; 30: 657-668
        • Cecchi M.
        • Capriles N.
        • Watson S.J.
        • Akil H.
        Beta1 adrenergic receptors in the bed nucleus of stria terminalis mediate differential responses to opiate withdrawal.
        Neuropsychopharmacology. 2007; 32: 589-599
        • Day H.E.
        • Curran E.J.
        • Watson Jr, S.J.
        • Akil H.
        Distinct neurochemical populations in the rat central nucleus of the amygdala and bed nucleus of the stria terminalis: Evidence for their selective activation by interleukin-1beta.
        J Comp Neurol. 1999; 413: 113-128
        • Rodaros D.
        • Caruana D.A.
        • Amir S.
        • Stewart J.
        Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area.
        Neuroscience. 2007; 150: 8-13
        • Erb S.
        • Rodaros S.
        A role for the CRF-containing pathway from central nucleus of the amygdala to bed nucleus of the stria terminalis in the stress-induced reinstatement of cocaine seeking in rats.
        Psychopharmacology. 2001; 158: 360-365
        • Phelix C.F.
        • Liposits Z.
        • Paull W.K.
        Catecholamine-CRF synaptic interaction in a septal bed nucleus: Afferents of neurons in the bed nucleus of the stria terminalis.
        Brain Res Bull. 1994; 33: 109-119
        • Vaughan J.
        • Donaldson C.
        • Bittencourt J.
        • Perrin M.H.
        • Lewis K.
        • Sutton S.
        • et al.
        Urocortin, a mammalian neuropeptide related to fish urotensin I and to corticotropin-releasing factor.
        Nature. 1995; 378: 287-292
        • Kourrich S.
        • Rothwell P.E.
        • Klug J.R.
        • Thomas M.J.
        Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens.
        J Neurosci. 2007; 27: 7921-7928
        • Saal D.
        • Dong Y.
        • Bonci A.
        • Malenka R.C.
        Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons.
        Neuron. 2003; 37: 577-582
        • Ungless M.A.
        • Whistler J.L.
        • Malenka R.C.
        • Bonci A.
        Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons.
        Nature. 2001; 411: 583-587
        • Fu Y.
        • Pollandt S.
        • Liu J.
        • Krishnan B.
        • Genzer K.
        • Orozco-Cabal L.
        • et al.
        Long-term potentiation (LTP) in the central amygdala (CeA) is enhanced after prolonged withdrawal from chronic cocaine and requires CRF1 receptors.
        J Neurophysiol. 2007; 97: 937-941
        • Francesconi W.
        • Berton F.
        • Repunte-Canonigo V.
        • Hagihara K.
        • Thurbon D.
        • Lekic D.
        • et al.
        Protracted withdrawal from alcohol and drugs of abuse impairs long-term potentiation of intrinsic excitability in the juxtacapsular bed nucleus of the stria terminalis.
        J Neurosci. 2009; 29: 5389-5401
        • Shaham Y.
        • Shalev U.
        • Lu L.
        • De Wit H.
        • Stewart J.
        The reinstatement model of drug relapse: History, methodology and major findings.
        Psychopharmacology (Berl). 2003; 168: 3-20
        • Carboni E.
        • Silvagni A.
        • Rolando M.T.
        • Di Chiara G.
        Stimulation of in vivo dopamine transmission in the bed nucleus of stria terminalis by reinforcing drugs.
        J Neurosci. 2000; 20 (RC102): RC102
        • Funk D.
        • Li Z.
        • Lê A.D.
        Effects of environmental and pharmacological stressors on c-fos and corticotropin-releasing factor mRNA in rat brain: Relationship to the reinstatement of alcohol seeking.
        Neuroscience. 2006; 138: 235-243
        • Ma S.
        • Morilak D.A.
        Norepinephrine release in medial amygdala facilitates activation of the hypothalamic-pituitary-adrenal axis in response to acute immobilisation stress.
        J Neuroendocrinol. 2005; 17: 22-28
        • Morilak D.A.
        • Barrera G.
        • Echevarria D.J.
        • Garcia A.S.
        • Hernandez A.
        • Ma S.
        • Petre C.O.
        Role of brain norepinephrine in the behavioral response to stress.
        Prog Neuropsychopharmacol Biol Psychiatry. 2005; 29: 1214-1224
        • Valjent E.
        • Pages C.
        • Herve D.
        • Girault J.A.
        • Caboche J.
        Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain.
        Eur J Neurosci. 2004; 19: 1826-1836
        • Park J.
        • Kile B.M.
        • Wightman R.M.
        In vivo voltammetric monitoring of norepinephrine release in the rat ventral bed nucleus of the stria terminalis and anteroventral thalamic nucleus.
        Eur J Neurosci. 2009; 30: 2121-2133
        • Deyama S.
        • Katayama T.
        • Ohno A.
        • Nakagawa T.
        • Kaneko S.
        • Yamaguchi T.
        • et al.
        Activation of the beta-adrenoceptor-protein kinase A signaling pathway within the ventral bed nucleus of the stria terminalis mediates the negative affective component of pain in rats.
        J Neurosci. 2008; 28: 7728-7736
        • Meloni E.G.
        • Jackson A.
        • Gerety L.P.
        • Cohen B.M.
        • Carlezon Jr, W.A.
        Role of the bed nucleus of the stria terminalis (BST) in the expression of conditioned fear.
        Ann N Y Acad Sci. 2006; 1071: 538-541
        • Phelix C.F.
        • Liposits Z.
        • Paull W.K.
        Monoamine innervation of bed nucleus of stria terminalis: An electron microscopic investigation.
        Brain Res Bull. 1992; 28: 949-965
        • Forray M.I.
        • Gysling K.
        Role of noradrenergic projections to the bed nucleus of the stria terminalis in the regulation of the hypothalamic-pituitary-adrenal axis.
        Brain Res Brain Res Rev. 2004; 47: 145-160
        • Jaferi A.
        • Lane D.A.
        • Pickel V.M.
        Subcellular plasticity of the corticotropin-releasing factor receptor in dendrites of the mouse bed nucleus of the stria terminalis following chronic opiate exposure.
        Neuroscience. 2009; 163: 143-154
        • Richter R.M.
        • Weiss F.
        In vivo CRF release in rat amygdala is increased during cocaine withdrawal in self-administering rats.
        Synapse. 1999; 32: 254-261
        • Maj M.
        • Turchan J.
        • Smialowska M.
        • Przewlocka B.
        Morphine and cocaine influence on CRF biosynthesis in the rat central nucleus of amygdala.
        Neuropeptides. 2003; 37: 105-110
        • Davis A.R.
        • Shields A.D.
        • Brigman J.L.
        • Norcross M.
        • McElligott Z.A.
        • Holmes A.
        • Winder D.G.
        Yohimbine impairs extinction of cocaine-conditioned place preference in an alpha2-adrenergic receptor independent process.
        Learn Mem. 2008; 15: 667-676
        • Olive M.F.
        • Koenig H.N.
        • Nannini M.A.
        • Hodge C.W.
        Elevated extracellular CRF levels in the bed nucleus of the stria terminalis during ethanol withdrawal and reduction by subsequent ethanol intake.
        Pharmacol Biochem Behav. 2002; 72: 213-220
        • Iredale P.A.
        • Alvaro J.D.
        • Lee Y.
        • Terwilliger R.
        • Chen Y.L.
        • Duman R.S.
        Role of corticotropin-releasing factor receptor-1 in opiate withdrawal.
        J Neurochem. 2000; 74: 199-208
        • Roberto M.
        • Cruz M.T.
        • Gilpin N.W.
        • Sabino V.
        • Schweitzer P.
        • Bajo M.
        • et al.
        Corticotropin releasing factor-induced amygdala gamma-aminobutyric acid release plays a key role in alcohol dependence.
        Biol Psychiatry. 2010; 67: 831-839
        • Blank T.
        • Nijholt I.
        • Grammatopoulos D.K.
        • Randeva H.S.
        • Hillhouse E.W.
        • Spiess J.
        Corticotropin-releasing factor receptors couple to multiple G-proteins to activate diverse intracellular signaling pathways in mouse hippocampus: Role in neuronal excitability and associative learning.
        J Neurosci. 2003; 23: 700-707
        • Liu J.
        • Yu B.
        • Orozco-Cabal L.
        • Grigoriadis D.E.
        • Rivier J.
        • Vale W.W.
        • et al.
        Chronic cocaine administration switches corticotropin-releasing factor2 receptor-mediated depression to facilitation of glutamatergic transmission in the lateral septum.
        J Neurosci. 2005; 25: 577-583
        • Guan X.
        • Zhang R.
        • Xu Y.
        • Li S.
        Cocaine withdrawal enhances long-term potentiation in rat hippocampus via changing the activity of corticotropin-releasing factor receptor subtype 2.
        Neuroscience. 2009; 161: 665-670
        • Erb S.
        • Stewart J.
        A role for the bed nucleus of the stria terminalis, but not the amygdala, in the effects of corticotropin-releasing factor on stress-induced reinstatement of cocaine seeking.
        J Neurosci. 1999; 19 (RC35): RC35
        • Wang J.
        • Fang Q.
        • Liu Z.
        • Lu L.
        Region-specific effects of brain corticotropin-releasing factor receptor type 1 blockade on footshock-stress- or drug-priming-induced reinstatement of morphine conditioned place preference in rats.
        Psychopharmacology (Berl). 2006; 185: 19-28