Corticotropin-releasing factor and noradrenergic signalling exert reciprocal control over startle reactivity

International Journal of Neuropsychopharmacology

Volumn 14, Issue 9, 2011, Pages 1179-1194

  Gresack, Jodi E ^a   Risbrough, Victoria B ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Corticotropin releasing hormone (CRH); CRF; norepinephrine; PTSD startle

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; ANTALARMIN; ATIPAMEZOLE; CIRAZOLINE; CLONIDINE; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; NORADRENALIN; PRAZOSIN; PROPRANOLOL; ADRENERGIC RECEPTOR; ALPHA 1 ADRENERGIC RECEPTOR BLOCKING AGENT; ALPHA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; ALPHA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; CORTICOTROPIN RELEASING FACTOR RECEPTOR; CRF RECEPTOR TYPE 1; NERVE PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; DOSE RESPONSE; DRUG EFFECT; MALE; MOUSE; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STARTLE REFLEX; ANIMAL; ANIMAL BEHAVIOR; BRAIN CORTEX; C57BL MOUSE; CHEMISTRY; DRUG ANTAGONISM; DRUG POTENTIATION; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; LOCUS CERULEUS; METABOLISM; NERVE CELL; NERVE CELL INHIBITION; PHYSIOLOGY; POSTTRAUMATIC STRESS DISORDER; SHEEP; SYNAPTIC TRANSMISSION;

ADRENERGIC ALPHA-1 RECEPTOR ANTAGONISTS; ADRENERGIC ALPHA-2 RECEPTOR AGONISTS; ADRENERGIC ALPHA-2 RECEPTOR ANTAGONISTS; ANIMALS; BEHAVIOR, ANIMAL; CEREBRAL CORTEX; CORTICOTROPIN-RELEASING HORMONE; INFUSIONS, INTRAVENTRICULAR; LOCUS COERULEUS; MALE; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEURAL INHIBITION; NEURONS; NOREPINEPHRINE; RECEPTORS, ADRENERGIC; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; SHEEP, DOMESTIC; STARTLE REACTION; STRESS DISORDERS, POST-TRAUMATIC; SYNAPTIC TRANSMISSION;

EID: 84856068779     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145710001409     Document Type: Article

References (76)

1. Adamec R, Fougere D, Risbrough V (2009). CRF receptor blockade prevents initiation and consolidation of stress effects on affect in the predator stress model of PTSD. International Journal of Neuropsychopharmacology 13, 1-11.
2. Adamec R, Muir C, Grimes M, Pearcey K (2007). Involvement of noradrenergic and corticoid receptors in the consolidation of the lasting anxiogenic effects of predator stress. Behavioural Brain Research 179, 192-207. (Pubitemid 46497456)
3. Alsene KM, Carasso BS, Connors EE, Bakshi VP (2006). Disruption of prepulse inhibition after stimulation of central but not peripheral alpha-1 adrenergic receptors. Neuropsychopharmacology 31, 2150-2161. (Pubitemid 44413192)
4. Astrachan DI, Gallager DW, Davis M (1983). Behavior and binding: desensitization to alpha 1-adrenergic stimulation of acoustic startle is associated with a decrease in alpha 1-adrenoceptor binding sites. Brain Research 276, 183-187. (Pubitemid 13006412)
5. Baker DG, West SA, Nicholson WE, Ekhator NN, et al. (1999). Serial CSF corticotropin-releasing hormone levels and adrenocortical activity in combat veterans with posttraumatic stress disorder. American Journal of Psychiatry 156, 585-588. (Pubitemid 29162980)
6. Bale TL, Vale WW (2003). Increased depression-like behaviors in corticotropin-releasing factor receptor-2-deficient mice: sexually dichotomous responses. Journal of Neuroscience 23, 5295-5301. (Pubitemid 36793258)
7. Barr AM, Powell SB, Markou A, Geyer MA (2006). Iloperidone reduces sensorimotor gating deficits in pharmacological models, but not a developmental model, of disrupted prepulse inhibition in rats. Neuropharmacology 51, 457-465. (Pubitemid 44215953)
8. Berridge CW, Dunn AJ (1989). Restraint-stress-induced changes in exploratory behavior appear to be mediated by norepinephrine-stimulated release of CRF. Journal of Neuroscience 9, 3513-3521. (Pubitemid 19260023)
9. Bremner JD, Licinio J, Darnell A, Krystal JH, et al. (1997). Elevated CSF corticotropin-releasing factor concentrations in posttraumatic stress disorder. American Journal of Psychiatry 154, 624-629. (Pubitemid 27197594)
10. Carasso BS, Bakshi VP, Geyer MA (1998). Disruption in prepulse inhibition after alpha-1 adrenoceptor stimulation in rats. Neuropharmacology 37, 401-404. (Pubitemid 28282646)
11. Conti LH, Sutherland JE, Muhlhauser CM (2009). Interaction between the effects of corticotropin-releasing factor and prepulse parameters on prepulse inhibition in two inbred rat strains and the F1 generation of a cross between them. Behavioural Brain Research 200, 165-172.
12. 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. Journal of Pharmacology and Experimental Therapeutics 281, 163-172. (Pubitemid 27203065)
13. Davis M (1980). Neurochemical modulation of sensorymotor reactivity : acoustic and tactile startle reflexes. Neuroscience and Biobehavioral Reviews 4, 241-263. (Pubitemid 10006360)
14. Davis M, Walker DL, Lee Y (1997). Roles of the amygdala and bed nucleus of the stria terminalis in fear and anxiety measured with the acoustic startle reflex. Possible relevance to PTSD. Annals of the New York Academy of Sciences 821, 305-331. (Pubitemid 27343031)
15. Dirks A, Groenink L, Westphal KG, Olivier JD, et al. (2003). Reversal of startle gating deficits in transgenic mice overexpressing corticotropin- releasing factor by antipsychotic drugs. Neuropsychopharmacology 28, 1790-1798. (Pubitemid 41070844)
16. Djouma E, Card K, Lodge DJ, Lawrence AJ (2006). The CRF1 receptor antagonist, antalarmin, reverses isolation-induced up-regulation of dopamine D2 receptors in the amygdala and nucleus accumbens of fawn-hooded rats. European Journal of Neuroscience 23, 3319-3327.
17. Dong HW, Swanson LW (2004). Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis. Journal of Comparative Neurology 468, 277-298. (Pubitemid 37490358)
18. Dunn AJ, Swiergiel AH, Palamarchouk V (2004). Brain circuits involved in corticotropin-releasing factornorepinephrine interactions during stress. Annals of the New York Academy of Science 1018, 25-34. (Pubitemid 38951387)
19. 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. Journal of Neuroscence 25, 5998-6004. (Pubitemid 40911431)
20. Forray MI, Gysling K, Andrés ME, Bustos G, et al. (2000). Medullary noradrenergic neurons projecting to the bed nucleus of the stria terminalis express mRNA for the NMDA-NR1 receptor. Brain Research Bulletin 52, 163-169. (Pubitemid 30261505)
21. Geracioti TD , Baker DG, Kasckow JW, Strawn JR, et al. (2008). Effects of trauma-related audiovisual stimulation on cerebrospinal fluid norepinephrine and corticotropinreleasing hormone concentrations in post-traumatic stress disorder. Psychoneuroendocrinology 33, 416-424.
22. Goldschmidt PL, Frances H, Simon P (1984). Stimulation of beta-adrenergic receptors and spontaneous motor activity in mice. Pharmacology, Biochemistry, and Behavior 21, 177-180. (Pubitemid 14071915)
23. Graham FK (1975). Presidential Address, 1974. The more or less startling effects of weak prestimulation. Psychophysiology 12, 238-248.
24. Griebel G, Simiand J, Steinberg R, Jung M, et al. (2002). 4-(2-Chloro-4-methoxy-5-methylphenyl)-N-[(1S)-2-cyclopropyl-1-(3-fluoro-4- methylphenyl)ethyl]5-methyl-N-(2-propynyl)-1,3-thiazol-2-amine hydrochloride (SSR125543A), a potent and selective corticotrophinreleasing factor(1) receptor antagonist. II. Characterization in rodent models of stress-related disorders. Journal of Pharmacology and Experimental Therapeutics 301, 333-345. (Pubitemid 34250312)
25. Grillon C (2008). Models and mechanisms of anxiety : evidence from startle studies. Psychopharmacology 199, 421-437.
26. Grillon C, Morgan III CA, Davis M, Southwick SM (1998). Effects of experimental context and explicit threat cues on acoustic startle in Vietnam veterans with posttraumatic stress disorder. Biological Psychiatry 44, 1027-1036. (Pubitemid 28545231)
27. Grillon C, Morgan CA, Southwick SM, Davis M, et al. (1996). Baseline startle amplitude and prepulse inhibition in Vietnam veterans with posttraumatic stress disorder. Psychiatry Research 64, 169-178. (Pubitemid 26380236)
28. Hauger RL, Risbrough V, Brauns O, Dautzenberg FM (2006). Corticotropin releasing factor (CRF) receptor signaling in the central nervous system: new molecular targets. CNS and Neurological Disorders : Drug Targets 5, 453-479. (Pubitemid 44203356)
29. Holstege G, Meiners L, Tan K (1985). Projections of the bed nucleus of the stria terminalis to the mesencephalon, pons, and medulla oblongata in the cat. Experimental Brain Research 58, 379-391. (Pubitemid 15114574)
30. Isogawa K, Akiyoshi J, Hikichi T, Yamamoto Y, et al. (2000). Effect of corticotropin releasing factor receptor 1 antagonist on extracellular norepinephrine, dopamine and serotonin in hippocampus and prefrontal cortex of rats in vivo. Neuropeptides 34, 234-239.
31. Izquierdo I, McGaugh JL (1985). Delayed onset of the amnestic effect of posttraining beta-endorphin : effects of propranolol administered prior to retention testing. European Journal of Pharmacology 113, 105-108. (Pubitemid 15246185)
32. Jeong KH, Jacobson L, Pacak K, Widmaier EP, et al. (2000). Impaired basal and restraint-induced epinephrine secretion in corticotropin-releasing hormone-deficient mice. Endocrinology 141, 1142-1150. (Pubitemid 32260457)
33. Jones BE, Yang TZ (1985). The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. Journal of Comparative Neurology 242, 56-92. (Pubitemid 16202793)
34. Koch M (1999). The neurobiology of startle. Progress in Neurobiology 59, 107-128. (Pubitemid 29425879)
35. Koob GF (1999). Corticotropin-releasing factor, norepinephrine, and stress. Biological Psychiatry 46, 1167-1180. (Pubitemid 30114435)
36. Krystal JH, Neumeister A (2009). Noradrenergic and serotonergic mechanisms in the neurobiology of posttraumatic stress disorder and resilience. Brain Research 1293, 13-23.
37. Lahdesmaki J, Sallinen J, MacDonald E, Scheinin M (2004). Alpha2A-adrenoceptors are important modulators of the effects of D-amphetamine on startle reactivity and brain monoamines. Neuropsychopharmacology 29, 1282-1293. (Pubitemid 38780651)
38. Lee EH, Chang SY, Chen AY (1994). CRF facilitates NE release from the hippocampus: a microdialysis study. Neuroscience Research 19, 327-330. (Pubitemid 24146912)
39. Lee Y, Davis M (1997). Role of the hippocampus, the bed nucleus of the stria terminalis, and the amygdala in the excitatory effect of corticotropin-releasing hormone on the acoustic startle reflex. Journal of Neuroscience 17, 6434-6446. (Pubitemid 27329915)
40. Lee Y, Lopez DE, Meloni EG, Davis M (1996). A primary acoustic startle pathway: obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis. Journal of Neuroscience 16, 3775-3789. (Pubitemid 26149513)
41. Liang KC, Melia KR, Miserendino MJ, Falls WA, et al. (1992). Corticotropin-releasing factor : long-lasting facilitation of the acoustic startle reflex. Journal of Neuroscience 12, 2303-2312.
42. Liu J, Yu B, Neugebauer V, Grigoriadis DE, et al. (2004). Corticotropin-releasing factor and Urocortin I modulate excitatory glutamatergic synaptic transmission. Journal of Neuroscience 24, 4020-4029. (Pubitemid 38544228)
43. Lorton D, Davis JN (1987). The distribution of beta-1-and beta-2-adrenergic receptors of normal and reeler mouse brain : an in vitro autoradiographic study. Neuroscience 23, 199-210. (Pubitemid 17159566)
44. Menon MK, Lloyd RL, Fitten LJ (1990). Antagonism of the hypothermic effect of clozapine in mice by centrally-active alpha 2-adrenergic antagonists and alpha 1-adrenergic agonists. Psychopharmacology 101, 67-72. (Pubitemid 20124744)
45. Morgan 3rd CA, Grillon C, Southwick SM, Nagy LM, et al. (1995). Yohimbine facilitated acoustic startle in combat veterans with post-traumatic stress disorder. Psychopharmacology 117, 466-471.
46. Okuyama S, Sakagawa T, Chaki S, Imagawa Y, et al. (1999). Anxiety-like behavior in mice lacking the angiotensin II type-2 receptor. Brain Research 821, 150-159. (Pubitemid 29219691)
47. Phelix CF, Liposits Z, Paull WK (1994). Catecholamine-CRF synaptic interaction in a septal bed nucleus: Afferents of neurons in the bed nucleus of the stria terminalis. Brain Research Bulletin 33, 109-119. (Pubitemid 124010120)
48. Pole N, Neylan TC, Otte C, Henn-Hasse C, et al. (2009). Prospective prediction of posttraumatic stress disorder symptoms using fear potentiated auditory startle responses. Biological Psychiatry 65, 235-240.
49. Reyes BA, Fox K, Valentino RJ, Van Bockstaele EJ (2006). Agonist-induced internalization of corticotropin-releasing factor receptors in noradrenergic neurons of the rat locus coeruleus. European Journal of Neuroscience 23, 2991-2998. (Pubitemid 43882878)
50. Risbrough VB, Geyer MA (2005). Anxiogenic treatments do not increase fear-potentiated startle in mice. Biological Psychiatry 57, 33-43. (Pubitemid 39647589)
51. Risbrough VB, Geyer MA, Hauger RL, Coste S, et al. (2009). CRF1 and CRF2 receptors are required for potentiated startle to contextual but not discrete cues. Neuropsychopharmacology 34, 1494-1503.
52. Risbrough VB, Hauger RL, Pelleymounter MA, Geyer MA (2003). Role of corticotropin releasing factor (CRF) receptors 1 and 2 in CRF-potentiated acoustic startle in mice. Psychopharmacology 170, 178-187. (Pubitemid 37421529)
53. Risbrough VB, Hauger RL, Roberts AL, Vale WW, et al. (2004). Corticotropin-releasing factor receptors CRF1 and CRF2 exert both additive and opposing influences on defensive startle behavior. Journal of Neuroscience 24, 6545-6552. (Pubitemid 38971703)
54. Risbrough VB, Stein MB (2006). Role of corticotropin releasing factor in anxiety disorders : a translational research perspective. Hormones and Behavior 50, 550-561. (Pubitemid 44307112)
55. Saha N, Datta H, Sharma PL (1991). Effects of morphine on memory: interactions with naloxone, propranolol and haloperidol. Pharmacology 42, 10-14.
56. Sallinen J, Haapalinna A, Viitamaa T, Kobilka BK, et al. (1998). Adrenergic alpha2C receptors modulate the acoustic startle reflex, prepulse inhibition, and aggression in mice. Journal of Neuroscience 18, 3035-3042. (Pubitemid 28163233)
57. Sautter FJ, Bissette G, Wiley J, Manguno-Mire G, et al. (2003). Corticotropin-releasing factor in posttraumatic stress disorder (PTSD) with secondary psychotic symptoms, nonpsychotic PTSD, and healthy control subjects. Biological Psychiatry 54, 1382-1388. (Pubitemid 37522162)
58. Schank JR, Liles LC & Weinshenker D (2008). Norepinephrine signaling through beta-adrenergic receptors is critical for expression of cocaine-induced anxiety. Biological Psychiatry 63, 1007-1012.
59. Schultz J, Daly JW (1973). Accumulation of cyclic adenosine 3k,5k-monophosphate in cerebral cortical slices from rat and mouse: Stimulatory effect of a-and b-adrenergic agents and adenosine. Journal of Neurochemistry 21, 1319-1326.
60. Shields AD, Wang Q, Winder DG (2009). alpha2Aadrenergic receptors heterosynaptically regulate glutamatergic transmission in the bed nucleus of the stria terminalis. Neuroscience 163, 339-351.
61. Shilling PD, Melendez G, Priebe K, Richelson E, et al. (2004). Neurotensin agonists block the prepulse inhibition deficits produced by a 5-HT2A and an alpha1 agonist. Psychopharmacology 175, 353-359. (Pubitemid 39361923)
62. Stevens DR, McCarley RW, Greene RW (1994). The mechanism of noradrenergic alpha 1 excitatory modulation of pontine reticular formation neurons. Journal of Neuroscience 14, 6481-6487. (Pubitemid 24333069)
63. Strawn JR & Geracioti TD (2008). Noradrenergic dysfunction and the psychopharmacology of posttraumatic stress disorder. Depression and Anxiety 25, 260-271. (Pubitemid 351499905)
64. Strazielle C, Lalonde R, Hébert C, Reade TA (1999). Regional brain distribution of noradrenaline uptake sites, and of a1-, a2-and b-adrenergic receptors in PCD mutant mice: a quantitative autoradiographic study. Neuroscience 94, 287-304. (Pubitemid 29457619)
65. Sutherland JE, Page ME, Conti LH (2008). The effect of corticotropin-releasing factor on prepulse inhibition is independent of serotonin in Brown Norway and Wistar-Kyoto rats. Pharmacology, Biochemistry, and Behavior 89, 324-337.
66. Swerdlow NR, Bongiovanni MJ, Tochen L, Shoemaker JM (2006). Separable noradrenergic and dopaminergic regulation of prepulse inhibition in rats : implications for predictive validity and Tourette Syndrome. Psychopharmacology 186, 246-254. (Pubitemid 43727342)
67. Swerdlow NR, Britton KT, Koob GF (1989). Potentiation of acoustic startle by corticotropin-releasing factor (CRF) and by fear are both reversed by alpha-helical CRF (9-41). Neuropsychopharmacology 2, 285-292. (Pubitemid 20025256)
68. Swerdlow NR, Geyer MA, Braff DL (2001). Neural circuit regulation of prepulse inhibition of startle in the rat : Current knowledge and future challenges. Psychopharmacology 156, 194-215. (Pubitemid 32702213)
69. Swerdlow NR, Geyer MA, Vale WW, Koob GF (1986). Corticotropin-releasing factor potentiates acoustic startle in rats : blockade by chlordiazepoxide. Psychopharmacology 88, 147-152. (Pubitemid 16148127)
70. Van Bockstaele EJ, Colago EE, Valentino RJ (1996). Corticotropin- releasing factor-containing axon terminals synapse onto catecholamine dendrites and may presynaptically modulate other afferents in the rostral pole of the nucleus locus coeruleus in the rat brain. Journal of Comparative Neurology 364, 523-534.
71. Van Pett K, Viau V, Bittencourt JC, Chan RK, et al. (2000). Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. Journal of Comparative Neurology 428, 191-212.
72. Varty GB, Bakshi VP, Geyer MA (1999). M100907, a serotonin 5-HT2A receptor antagonist and putative antipsychotic, blocks dizocilpine-induced prepulse inhibition deficits in Sprague-Dawley and Wistar rats. Neuropsychopharmacology 20, 311-321. (Pubitemid 29099762)
73. Vinkers CH, Risbrough VB, Geyer MA, Caldwell S, et al. (2007). Role of dopamine D1 and D2 receptors in CRFinduced disruption of sensorimotor gating. Pharmacology, Biochemistry, and Behavior 86, 550-558. (Pubitemid 46466888)
74. Vythilingam M, Anderson GM, Owens MJ, Halasznski TM, et al. (2000). Cerebrospinal fluid corticotropin-releasing hormone in healthy humans: effects of yohimbine and naloxone. Journal of Clinical Endocrinology and Metabolism 85, 4138-4145. (Pubitemid 32055365)
75. Walker DL, Miles LA, Davis M (2009). Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like vs. phasic fear-like responses. Progress in Neuropsychopharmacology and Biological Psychiatry 33, 1291-1308.
76. Zarrindast MR, Haidari H, Jafari MR, Djahanguiri B (2004). Influence of beta-adrenoceptor agonists and antagonists on baclofen-induced memory impairment in mice. Behavioral Pharmacology 15, 293-297. (Pubitemid 39062559)