Both α1- and β1-adrenoceptors in the bed nucleus of the stria terminalis are involved in the expression of conditioned contextual fear

British Journal of Pharmacology

Volumn 167, Issue 1, 2012, Pages 207-221

  Hott, Sara C ^a   Gomes, Felipe V ^a   Fabri, Denise R S ^a   Reis, Daniel G ^a   Crestani, Carlos C ^b   Côrrea, Fernando M A ^a   Resstel, Leonardo B M ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

adrenoceptor antagonists; autonomic responses; cardiovascular system; conditioned emotional responses; noradrenergic system

Indexed keywords

2 (2 METHOXY 1,4 BENZODIOXAN 2 YL) 2 IMIDAZOLINE; 2 [[2 (2,6 DIMETHOXYPHENOXY)ETHYL]AMINOMETHYL] 1,4 BENZODIOXAN; 3 ISOPROPYLAMINO 1 (7 METHYL 4 INDANYLOXY) 2 BUTANOL; 5 [2 [[2 HYDROXY 3 [4 (1 METHYL 4 TRIFLUOROMETHYL 2 IMIDAZOLYL)PHENOXY]PROPYL]AMINO]ETHOXY]SALICYLAMIDE; ALPHA 1 ADRENERGIC RECEPTOR; BETA 1 ADRENERGIC RECEPTOR; PHENTOLAMINE; PROPRANOLOL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVE; AVERSION; BED NUCLEUS OF THE STRIA TERMINALIS; BEHAVIOR; CONDITIONING; CONTROLLED STUDY; FEAR; FOOTSHOCK; FREEZING; HEART RATE; LIMBIC SYSTEM; MALE; MEAN ARTERIAL PRESSURE; NERVE POTENTIAL; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; NORADRENERGIC TRANSMISSION; PRIORITY JOURNAL; RAT; SKIN TEMPERATURE;

ADRENERGIC ALPHA-ANTAGONISTS; ADRENERGIC BETA-ANTAGONISTS; ANIMALS; CONDITIONING (PSYCHOLOGY); DIOXANES; ELECTROSHOCK; FEAR; IDAZOXAN; IMIDAZOLES; MALE; PHENTOLAMINE; PROPANOLAMINES; PROPRANOLOL; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, ALPHA-1; RECEPTORS, ADRENERGIC, BETA-1; SEPTAL NUCLEI;

EID: 84864656568     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.01985.x     Document Type: Article

References (69)

1. Alexander SP, Mathie A, Peters JA, (2011). Guide to receptors and channels (GRAC), 5th edition. Br J Pharmacol 164 (Suppl 1): S1-S324.
2. Alheid GF, (2003). Extended amygdala and basal forebrain. Ann N Y Acad Sci 985: 185-205.
3. Alves FH, Resstel LB, Correa FM, Crestani CC, (2011). Bed nucleus of the stria terminalis alpha1- and alpha2-adrenoceptors differentially modulate the cardiovascular responses to exercise in rats. Neuroscience 177: 74-83.
4. Antoniadis EA, McDonald RJ, (1999). Discriminative fear conditioning to context expressed by multiple measures of fear in the rat. Behav Brain Res 101: 1-13.
5. Aston-Jones G, Rajkowski J, Cohen J, (1999). Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry 46: 1309-1320.
6. Beck CH, Fibiger HC, (1995). Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment. J Neurosci 15: 709-720.
7. Blanchard RJ, Blanchard DC, (1969). Crouching as an index of fear. J Comp Physiol Psychol 67: 370-375.
8. Blessing WW, (2003). Lower brainstem pathways regulating sympathetically mediated changes in cutaneous blood flow. Cell Mol Neurobiol 23: 527-538.
9. Bylund DB, Eikenberg DC, Hieble JP, Langer SZ, Lefkowitz RJ, Minneman KP, et al,. (1994). International Union of Pharmacology nomenclature of adrenoceptors. Pharmacol Rev 46: 121-136.
10. Carrive P, (2000). Conditioned fear to environmental context: cardiovascular and behavioral components in the rat. Brain Res 858: 440-445.
11. Carrive P, (2002). Cardiovascular and behavioural components of conditioned fear to context after ganglionic and alpha-adrenergic blockade. Auton Neurosci 98: 90-93.
12. Casada JH, Dafny N, (1991). Restraint and stimulation of bed nucleus of the stria terminalis produce similar stress-like behaviors. Brain Res Bull 27: 207-212.
13. 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.
14. Cecchi M, Capriles N, Watson SJ, Akil H, (2007). Beta1 adrenergic receptors in the bed nucleus of stria terminalis mediate differential responses to opiate withdrawal. Neuropsychopharmacology 32: 589-599.
15. Crestani CC, Alves FH, Resstel LB, Correa FM, (2008a). Bed nucleus of the stria terminalis alpha(1)-adrenoceptor modulates baroreflex cardiac component in unanesthetized rats. Brain Res 1245: 108-115.
16. Crestani CC, Alves FH, Resstel LB, Correa FM, (2008b). Both alpha1 and alpha2-adrenoceptors mediate the cardiovascular responses to noradrenaline microinjected into the bed nucleus of the stria terminal of rats. Br J Pharmacol 153: 583-590.
17. Crestani CC, Alves FH, Tavares RF, Correa FM, (2009). Role of the bed nucleus of the stria terminalis in the cardiovascular responses to acute restraint stress in rats. Stress 12: 268-278.
18. Davis M, Walker DL, Miles L, Grillon C, (2010). Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 35: 105-135.
19. 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.
20. Deyama S, Katayama T, Ohno A, Nakagawa T, Kaneno S, Yamaguchi T, et al,. (2008). 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 28: 7728-7736.
21. Deyama S, Katayama T, Kondoh N, Nakagawa T, Kaneno S, Yamaguchi T, et al,. (2009). Role of enhanced noradrenergic transmission within the ventral bed nucleus of the stria terminalis in visceral pain-induced aversion in rats. Behav Brain Res 197: 279-283.
22. Do-Monte FH, Allensworth M, Carobrez AP, (2010a). Impairment of contextual conditioned fear extinction after microinjection of alpha-1-adrenergic blocker prazosin into the medial prefrontal cortex. Behav Brain Res 211: 89-95.
23. Do-Monte FH, Kincheski GC, Pavesi E, Sordi R, Assreuy J, Carobrez AP, (2010b). Role of beta-adrenergic receptors in the ventromedial prefrontal cortex during contextual fear extinction in rats. Neurobiol Learn Mem 94: 318-328.
24. Dong HW, Swanson LW, (2004). Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis. J Comp Neurol 468: 277-298.
25. Dong HW, Petrovich GD, Swanson LW, (2001a). Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Brain Res Rev 38: 192-246.
26. Dong HW, Petrovich GD, Watts AG, Swanson LW, (2001b). Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain. J Comp Neurol 436: 430-455.
27. 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.
28. Dunn JD, (1987). Plasma corticosterone responses to electrical stimulation of the bed nucleus of the stria terminalis. Brain Res 407: 327-331.
29. Dunn JD, Williams TJ, (1995). Cardiovascular responses to electrical stimulation of the bed nucleus of the stria terminalis. J Comp Neurol 352: 227-234.
30. Egli RE, Kash TL, Choo K, Savchenko V, Matthews RT, Blakely RD, et al,. (2005). Norepinephrine modulates glutamatergic transmission in the bed nucleus of the stria terminalis. Neuropsychopharmacology 30: 657-668.
31. Fanselow MS, (1980). Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci 15: 177-182.
32. Fendt M, Siegl S, Steiniger-Brach B, (2005). Noradrenaline transmission within the ventral bed nucleus of the stria terminalis is critical for fear behavior induced by trimethylthiazoline, a component of fox odor. J Neurosci 25: 5998-6004.
33. 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.
34. Forray MI, Bustos G, Gysling K, (1997). Regulation of norepinephrine release from the rat bed nucleus of the stria terminalis: in vivo microdialysis studies. J Neurosci Res 50: 1040-1046.
35. Frank J, Witte K, Schrodl W, Schutt C, (2004). Chronic alcoholism causes deleterious conditioning of innate immunity. Alcohol Alcohol 39: 386-392.
36. Fuentealba JA, Forray MI, Gysling K, (2000). Chronic morphine treatment and withdrawal increase extracellular levels of norepinephrine in the rat bed nucleus of the stria terminalis. J Neurochem 75: 741-748.
37. Giancola SB, Roder S, Ciriello J, (1993). Contribution of caudal ventrolateral medulla to the cardiovascular responses elicited by activation of bed nucleus of the stria terminalis. Brain Res 606: 162-166.
38. Gomes FV, Reis DG, Alves FH, Correa FM, Guimarães FS, Resstel LB, (2012). Cannabidiol injected into the bed nucleus of the stria terminalis reduces the expression of contextual fear conditioning via 5-HT1A receptors. J Psychopharmacol 26: 104-113.
39. Gordon CJ, (1990). Thermal biology of the laboratory rat. Physiol Behav 47: 963-991.
40. Grillon C, Cordova J, Morgan CA, Charney DS, Davis M, (2004). Effects of the beta-blocker propranolol on cued and contextual fear conditioning in humans. Psychopharmacology (Berl) 175: 342-352.
41. Herman JP, Cullinan WE, Watson SJ, (1994). Involvement of the bed nucleus of the stria terminalis in tonic regulation of paraventricular hypothalamic CRH and AVP mRNA expression. J Neuroendocrinol 6: 433-442.
42. Lazzaro SC, Hou M, Cunha C, LeDoux JE, Cain CK, (2010). Antagonism of lateral amygdala alpha1-adrenergic receptors facilitates fear conditioning and long-term potentiation. Learn Mem 17: 489-493.
43. MacNaughton N, Corr PJ, (2004). A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci Biobehav Rev 28: 285-305.
44. Mccarty R, Kopin IJ, (1978). Alterations in plasma catecholamines and behavior during acute stress in spontaneously hypertensive and Wistar-Kyoto normotensive rats. Life Sci 22: 997-1005.
45. McElligott ZA, Winder DG, (2008). 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 33: 2313-2323.
46. McGrath J, Drummond G, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
47. Miralles A, Olmos G, Sastre M, Barturen F, Martin I, Garcia-Sevilla JA, (1993). Discrimination and pharmacological characterization of I2-imidazoline sites with [3H]idazoxan and alpha-2 adrenoceptors with [3H]RX821002 (2-methoxy idazoxan) in the human and rat brains. J Pharmacol Exp Ther 264: 1187-1197.
48. Moore RY, (1978). Catecholamin innervation of the basal forebrain. I. The septal area. J Comp Neurol 177: 665-684.
49. Morilak DA, Barrera G, Echevarria DJ, Garcia AS, Hernandez A, Ma S, et al,. (2005). Role of brain norepinephrine in the behavioral response to stress. Prog Neuropsychopharmacol Biol Psychiatry 29: 1214-1224.
50. Murchison CF, Schutsky K, Jin SH, Thomas SA, (2011). Norepinephrine and ss-adrenergic signaling facilitate activation of hippocampal CA1 pyramidal neurons during contextual memory retrieval. Neuroscience 181: 109-116.
51. Nijsen MJ, Croiset G, Diamant M, Stam R, Delsing D, de Wied D, et al,. (1998). Conditioned fear-induced tachycardia in the rat: vagal involvement. Eur J Pharmacol 350: 211-222.
52. 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 corticotrophin-releasing factor receptor-dependent and cocaine-regulated mechanism. Biol Psychiatry 69: 1083-1090.
53. Onaka T, Yagi K, (1998). Role of noradrenergic projections to the bed nucleus of the stria terminalis in neuroendocrine and behavioral responses to fear-related stimuli in rats. Brain Res 788: 287-293.
54. Ouyang M, Thomas SA, (2005). A requirement for memory retrieval during and after long-term extinction learning. Proc Natl Acad Sci U S A 102: 9347-9352.
55. Pacak K, McCarty R, Palkovits M, Kopin IJ, Goldstein DS, (1995). Effects of immobilization on in vivo release of norepinephrine in the bed nucleus of the stria terminalis in conscious rats. Brain Res 688: 242-246.
56. Paxinos G, Watson C, (1997). The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press: Sydney.
57. Peskind ER, Bonner LT, Hoff DJ, Raskind MA, (2003). Prazosin reduces trauma-related nightmares in older men with chronic posttraumatic stress disorder. J Geriatr Psychiatry Neurol 16: 165-171.
58. Radley JJ, Gosselink KL, Sawchenko PE, (2009). A discrete GABAergic relay mediates medial prefrontal cortical inhibition of the neuroendocrine stress response. J Neurosci 29: 7330-7340.
59. Ressler KJ, Nemeroff CB, (2000). Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress Anxiety 12 (Suppl 1): 2-19.
60. Resstel LB, Alves FH, Reis DG, Crestani CC, Correa FM, Guimaraes FS, (2008). Anxiolytic-like effects induced by acute reversible inactivation of the bed nucleus of stria terminalis. Neuroscience 154: 869-876.
61. Sullivan GM, Apergis J, Bush DE, Johnson LR, Hou M, Ledoux JE, (2004). Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus. Neuroscience 128: 7-14.
62. Sved AF, Ito S, Madden CJ, (2000). Baroreflex dependent and independent roles of the caudal ventrolateral medulla in cardiovascula regulation. Brain Res Bull 51: 129-133.
63. Swanson LW, Hartman BK, (1975). The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker. J Comp Neurol 163: 467-505.
64. Vertes RP, (2006). Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142: 1-20.
65. Vianna DM, Carrive P, (2005). Changes in cutaneous and body temperature during and after conditioned fear to context in the rat. Eur J Neurosci 21: 2505-2512.
66. Walker DL, Toufexis DJ, Davis M, (2003). Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463: 199-216.
67. Yancey SL, Overton JM, (1993). Cardiovascular responses to voluntary and treadmill exercise in rats. J Appl Physiol 75: 1334-1340.
68. Zhou XJ, Yang J, Yan FL, Wang DX, Li XY, Fan XQ, et al,. (2010). Norepinephrine plays an important role in antinociceptive modulation of hypothalamic paraventricular nucleus in the rat. Int J Neurosci 120: 428-438.
69. Zimmerman JM, Rabinak CA, McLachlan IG, Maren S, (2007). The central nucleus of the amygdala is essential for acquiring and expressing conditional fear after overtraining. Learn Mem 14: 634-644.