Noradrenergic synaptic function in the bed nucleus of the stria terminalis varies in animal models of anxiety and addiction

Neuropsychopharmacology

Volumn 38, Issue 9, 2013, Pages 1665-1673

  McElligott, Zoé A ^a,b   Fox, Megan E ^a   Walsh, Paul L ^a   Urban, Daniel J ^b   Ferrel, Martilias S ^b   Roth, Bryan L ^b   Mark Wightman, R ^a,b  

^a The University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

bed nucleus of the stria terminalis; morphine; neuronal release; Norepinephrine; norepinephrine uptake

Indexed keywords

MORPHINE; NORADRENALIN;

ADDICTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; DRUG USE; LEWIS RAT; MOOD DISORDER; MORPHINE ADDICTION; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; RAT; SPRAGUE DAWLEY RAT; STRIA TERMINALIS; SYNAPTIC TRANSMISSION;

ADRENERGIC NEURONS; ANIMALS; ANXIETY; DOPAMINE; MALE; MAZE LEARNING; MORPHINE DEPENDENCE; NOREPINEPHRINE; RATS; RATS, INBRED LEW; RATS, SPRAGUE-DAWLEY; SEPTAL NUCLEI; SPECIES SPECIFICITY; SUBSTANCE WITHDRAWAL SYNDROME; SYNAPTIC TRANSMISSION;

EID: 84880327874     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.63     Document Type: Article

References (40)

1. Amitai N, Liu J, Schulteis G (2006). Discrete cues paired with naloxone-precipitated withdrawal from acute morphine dependence elicit conditioned withdrawal responses. Behav Pharmacol 17: 213-222.
2. Armstrong JM, Lefevre-Borg F, Scatton B, Cavero I (1982). Urethane inhibits cardiovascular responses mediated by the stimulation of alpha-2 adrenoceptors in the rat. J Pharmacol Exp Ther 223: 524-535. (Pubitemid 12005758)
3. Cecchi M, Khoshbouei H, Javors M, Morilak DA (2002). Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress. Neuroscience 112: 13-21. (Pubitemid 34603494)
4. Cohen H, Zohar J, Gidron Y, Matar MA, Belkind D, Loewenthal U et al (2006). Blunted HPA axis response to stress influences susceptibility to posttraumatic stress response in rats. Biol Psychiatry 59: 1208-1218.
5. Delfs JM, Zhu Y, Druhan JP, Aston-Jones G (2000). Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion. Nature 403: 430-434. (Pubitemid 30073092)
6. Drolet G (2009). Progress in Neuro-Psychopharmacology and Biological Psychiatry. Elsevier Inc: Amsterdam.
7. Dumont EC, Williams JT (2004). Noradrenaline triggers GABAA inhibition of bed nucleus of the stria terminalis neurons projecting to the ventral tegmental area. J Neurosci 24: 8198-8204. (Pubitemid 39280798)
8. Duvarci S, Bauer EP, Pare D (2009). The bed nucleus of the stria terminalis mediates inter-individual variations in anxiety and fear. J Neurosci 29: 10357-10361.
9. Erb S, Hitchcott PK, Rajabi H, Mueller D, Shaham Y, Stewart J (2000). Alpha-2 adrenergic receptor agonists block stressinduced reinstatement of cocaine seeking. Neuropsychopharmacology 23: 138-150. (Pubitemid 30406898)
10. Forray MI, Gysling K (2004). 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 47: 145-160. (Pubitemid 39574317)
11. Gasser PJ, Orchinik M, Raju I, Lowry CA (2009). Distribution of organic cation transporter 3, a corticosterone-sensitive monoamine transporter, in the rat brain. J Compar Neurol 512: 529-555.
12. George FR, Goldberg SR (1989). Genetic approaches to the analysis of addiction processes. Trends Pharmacol Sci 10: 78-83. (Pubitemid 19059715)
13. Heilig M, Egli M (2006). Pharmacological treatment of alcohol dependence: target symptoms and target mechanisms. Pharmacol Ther 111: 855-876. (Pubitemid 44118437)
14. Herr NR, Park J, McElligott ZA, Belle AM, Carelli RM, Wightman RM (2012). In vivo voltammetry monitoring of electrically evoked extracellular norepinephrine in subregions of the bed nucleus of the stria terminalis. J Neurophysiol 107: 1731-1737.
15. Hyman SM, Hong KI, Chaplin TM, Dabre Z, Comegys AD, Kimmerling A et al (2009). A stress-coping profile of opioid dependent individuals entering naltrexone treatment: a comparison with healthy controls. Psychol Addict Behav 23: 613-619.
16. John CE, Budygin EA, Mateo Y, Jones SR (2006). Neurochemical characterization of the release and uptake of dopamine in ventral tegmental area and serotonin in substantia nigra of the mouse. J Neurochem 96: 267-282.
17. Koob GF (2009). Brain stress systems in the amygdala and addiction. Brain Res 1293: 61-75.
18. Koob GF, Volkow ND (2010). Neurocircuitry of addiction. Neuropsychopharmacology 35: 217-238.
19. Leri F, Flores J, Rodaros D, Stewart J (2002). Blockade of stressinduced 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 22: 5713-5718. (Pubitemid 35386493)
20. McElligott ZA, Klug JR, Nobis WP, Patel S, Grueter BA, Kash TL et al (2010). Distinct forms of Gq-receptor-dependent plasticity of excitatory transmission in the BNST are differentially affected by stress. Proc Natl Acad Sci USA 107: 2271-2276.
21. McElligott ZA, Winder DG (2008). Alpha1-adrenergic receptorinduced heterosynaptic long-term depression in the bed nucleus of the stria terminalis is disrupted in mouse models of affective disorders. Neuropsychopharmacology 33: 2313-2323.
22. McElligott ZA, Winder DG (2009). Modulation of glutamatergic synaptic transmission in the bed nucleus of the stria terminalis. Prog Neuropsychopharmacol Biol Psychiatry 33: 1329-1335.
23. Meloni EG, Gerety LP, Knoll AT, Cohen BM, Carlezon Jr WA (2006). Behavioral and anatomical interactions between dopamine and corticotropin- releasing factor in the rat. J Neurosci 26: 3855-3863.
24. Montague PR, McClure SM, Baldwin PR, Phillips PE, Budygin EA, Stuber GD et al (2004). Dynamic gain control of dopamine delivery in freely moving animals. J Neurosci 24: 1754-1759. (Pubitemid 38240973)
25. Nobis WP, Kash TL, Silberman Y, Winder DG (2011). beta-Adrenergic receptors enhance excitatory transmission in the bed nucleus of the stria terminalis through a corticotrophinreleasing factor receptor-dependent and cocaine-regulated mechanism. Biological psychiatry 69: 1083-1090.
26. Pardon MC, Gould GG, Garcia A, Phillips L, Cook MC, Miller SA et al (2002). Stress reactivity of the brain noradrenergic system in three rat strains differing in their neuroendocrine and behavioral responses to stress: implications for susceptibility to stress-related neuropsychiatric disorders. Neuroscience 115: 229-242. (Pubitemid 35232702)
27. Park J, Kile BM, Wightman RM (2009). In vivo voltammetric monitoring of norepinephrine release in the rat ventral bed nucleus of the stria terminalis and anteroventral thalamic nucleus. Eur J Neurosci 30: 2121-2133.
28. Park J, Wheeler RA, Fontillas K, Keithley RB, Carelli RM, Wightman RM (2012). Catecholamines in the bed nucleus of the stria terminalis reciprocally respond to reward and aversion. Biol Psychiatry 71: 327-334.
29. Picetti R, Caccavo JA, Ho A, Kreek MJ (2012). Dose escalation and dose preference in extended-access heroin self-administration in Lewis and Fischer rats. Psychopharmacology 220: 163-172.
30. Raskind MA, Dobie DJ, Kanter ED, Petrie EC, Thompson CE, Peskind ER (2000). The alpha1-adrenergic antagonist prazosin ameliorates combat trauma nightmares in veterans with posttraumatic stress disorder: a report of 4 cases. J Clin Psychiatry 61: 129-133. (Pubitemid 30141645)
31. Sanchez-Cardoso P, Higuera-Matas A, Martin S, del Olmo N, Miguens M, Garcia-Lecumberri C et al (2007). Modulation of the endogenous opioid system after morphine self-administration and during its extinction: a study in Lewis and Fischer 344 rats. Neuropharmacology 52: 931-948. (Pubitemid 46237637)
32. Schulteis G, Heyser CJ, Koob GF (1999). Differential expression of response-disruptive and somatic indices of opiate withdrawal during the initiation and development of opiate dependence. Behav Pharmacol 10: 235-242. (Pubitemid 29301260)
33. Simpson TL, Saxon AJ, Meredith CW, Malte CA, McBride B, Ferguson LC et al (2008). A pilot trial of the alpha-1 adrenergic antagonist, Prazosin, for alcohol dependence. Alcohol Clin Exp Res 33: 255-263.
34. Sinha R (2008). Chronic stress, drug use, and vulnerability to addiction. Ann N Y Acad Sci 1141: 105-130.
35. Trendelenburg AU, Klebroff W, Hein L, Starke K (2001). A study of presynaptic alpha2-autoreceptors in alpha2A/D-, alpha2B-and alpha2C- adrenoceptor-deficient mice. Naunyn-Schmiedeberg Arch Pharmacol 364: 117-130.
36. Trescot AM, Datta S, Lee M, Hansen H (2008). Opioid pharmacology. Pain Physician 11(2 Suppl): S133-S153. (Pubitemid 351682083)
37. Wang X, Cen X, Lu L (2001). Noradrenaline in the bed nucleus of the stria terminalis is critical for stress-induced reactivation of morphine-conditioned place preference in rats. Eur J Pharmacol 432: 153-161. (Pubitemid 34003596)
38. Wightman RM, Amatore C, Engstrom RC, Hale PD, Kristensen EW, Kuhr WG et al (1988). Real-time characterization of dopamine overflow and uptake in the rat striatum. Neuroscience 25: 513-523.
39. Xu F, Gainetdinov RR, Wetsel WC, Jones SR, Bohn LM, Miller GW et al (2000). Mice lacking the norepinephrine transporter are supersensitive to psychostimulants. Nat Neurosci 3: 465-471. (Pubitemid 30495628)
40. Yorgason JT, Espana RA, Jones SR (2011). Demon voltammetry and analysis software: analysis of cocaine-induced alterations in dopamine signaling using multiple kinetic measures. J Neurosci Methods 202: 158-164.