Repeated stressor exposure enhances contextual fear memory in a beta-adrenergic receptor-dependent process and increases impulsivity in a non-beta receptor-dependent fashion

Physiology and Behavior

Volumn 150, Issue , 2015, Pages 64-68

  Camp, Robert M ^a   Johnson, John D ^a  

^a KENT STATE UNIVERSITY   (United States)

Author keywords

Associative learning; Chronic mild stress; Contextual fear conditioning; Norepinephrine; Passive avoidance; Propranolol

Indexed keywords

BETA ADRENERGIC RECEPTOR; PROPRANOLOL; BETA ADRENERGIC RECEPTOR BLOCKING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BEHAVIOR CHANGE; CHRONIC STRESS; CONTROLLED STUDY; DECISION MAKING; FEAR; FOOTSHOCK; FREEZING; IMPULSIVENESS; LOCOMOTION; MEMORY; NONHUMAN; PASSIVE AVOIDANCE; PRIORITY JOURNAL; RAT; STATE DEPENDENT LEARNING; ANALYSIS OF VARIANCE; ANIMAL; AVOIDANCE BEHAVIOR; CATALEPSY; CONDITIONING; DRUG EFFECTS; EXPLORATORY BEHAVIOR; FISCHER 344 RAT; MALE; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADRENERGIC BETA-ANTAGONISTS; ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; CONDITIONING (PSYCHOLOGY); EXPLORATORY BEHAVIOR; FEAR; FREEZING REACTION, CATALEPTIC; IMPULSIVE BEHAVIOR; MALE; MEMORY; PROPRANOLOL; RATS; RATS, INBRED F344; RECEPTORS, ADRENERGIC, BETA; STRESS, PSYCHOLOGICAL;

EID: 84939565619     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2015.03.008     Document Type: Article

References (42)

1. Cordero M.I., Venero C., Kruyt N.D., Sandi C. Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats. Horm. Behav. Nov. 2003, 44(4):338-345.
2. Shors T.J., Weiss C., Thompson R.F. Stress-induced facilitation of classical conditioning. Science 1992, 257(5069):537-539. (80-).
3. Blanchard R.J., Blanchard D.C. Crouching as an index of fear. J. Comp. Physiol. Psychol. Mar. 1969, 67(3):370-375.
4. Shors T.J. Acute stress rapidly and persistently enhances memory formation in the male rat. Neurobiol. Learn. Mem. Jan. 2001, 75(1):10-29.
5. Ferry B., Roozendaal B., McGaugh J.L. Role of norepinephrine in mediating stress hormone regulation of long-term memory storage: a critical involvement of the amygdala. Biol. Psychiatry Nov. 1999, 46(9):1140-1152.
6. Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nat. Rev. Neurosci. Jun. 2009, 10(6):423-433.
7. Roozendaal B., McGaugh J.L. Memory modulation. Behav. Neurosci. Dec. 2011, 125(6):797-824.
8. Dębiec J., LeDoux J.E. Noradrenergic signaling in the amygdala contributes to the reconsolidation of fear memory: treatment implications for PTSD. Ann. N. Y. Acad. Sci. Jul. 2006, 1071(1):521-524.
9. Hatfield T., McGaugh J.L. Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiol. Learn. Mem. Mar. 1999, 71(2):232-239.
10. Quirarte G.L., Roozendaal B., McGaugh J.L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc. Natl. Acad. Sci. U. S. A. Dec. 1997, 94(25):14048-14053.
11. LaLumiere R.T., Buen T.-V., McGaugh J.L. Post-training intra-basolateral amygdala infusions of norepinephrine enhance consolidation of memory for contextual fear conditioning. J. Neurosci. Jul. 2003, 23(17):6754-6758.
12. Introini-Collison I., Saghafi D., Novack G., McGaugh J. Memory-enhancing effects of post-training dipivefrin and epinephrine: involvement of peripheral and central adrenergic receptors. Brain Res. 1992, 572(1-2):81-86.
13. Sarabdjitsingh R.A., Kofink D., Karst H., de Kloet E.R., Joëls M. Stress-induced enhancement of mouse amygdalar synaptic plasticity depends on glucocorticoid and ß-adrenergic activity. PLoS One Jan. 2012, 7(8):e42143.
14. Hubbard D.T., Nakashima B.R., Lee I., Takahashi L.K. Activation of basolateral amygdala corticotropin-releasing factor 1 receptors modulates the consolidation of contextual fear. Neuroscience Dec. 2007, 150(4):818-828.
15. Roozendaal B., Brunson K.L., Holloway B.L., McGaugh J.L., Baram T.Z. Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proc. Natl. Acad. Sci. U. S. A. Oct. 2002, 99(21):13908-13913.
16. Roozendaal B., Quirarte G.L., McGaugh J.L. Glucocorticoids interact with the basolateral amygdala beta-adrenoceptor-cAMP/PKA system in influencing memory consolidation. Eur. J. Neurosci. Feb. 2002, 15(3):553-560.
17. Roozendaal B., Schelling G., McGaugh J.L. Corticotropin-releasing factor in the basolateral amygdala enhances memory consolidation via an interaction with the beta-adrenoceptor-cAMP pathway: dependence on glucocorticoid receptor activation. J. Neurosci. Jun. 2008, 28(26):6642-6651.
18. Porterfield V.M., Gabella K.M., Simmons M.A., Johnson J.D. Repeated stressor exposure regionally enhances beta-adrenergic receptor-mediated brain IL-1β production. Brain Behav. Immun. Nov. 2012, 26(8):1249-1255.
19. D'Aquila P.S., Brain P., Willner P. Effects of chronic mild stress on performance in behavioural tests relevant to anxiety and depression. Physiol. Behav. Nov. 1994, 56(5):861-867.
20. Kompagne H., Bárdos G., Szénási G., Gacsályi I., Hársing L.G., Lévay G. Chronic mild stress generates clear depressive but ambiguous anxiety-like behaviour in rats. Behav. Brain Res. Nov. 2008, 193(2):311-314.
21. Mineur Y.S., Belzung C., Crusio W.E. Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behav. Brain Res. Nov. 2006, 175(1):43-50.
22. Fendt M., Endres T., Apfelbach R. Temporary inactivation of the bed nucleus of the stria terminalis but not of the amygdala blocks freezing induced by trimethylthiazoline, a component of fox feces. J. Neurosci. Jan. 2003, 23(1):23-28.
23. Camp R.M., Remus J.L., Kalburgi S.N., Porterfield V.M., Johnson J.D. Fear conditioning can contribute to behavioral changes observed in a repeated stress model. Behav. Brain Res. 2012, 233(2):536-544.
24. Johnson J.D., Campisi J., Sharkey C.M., Kennedy S.L., Nickerson M., Greenwood B.N., Fleshner M. Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience Jan. 2005, 135(4):1295-1307.
25. Kompagne H., Bárdos G., Szénázy G., Gacsályi I., Hársing L., Lévay G. Chronic mild stress generates clear depressive but ambiguous anxiety-like behaviour in rats. Behav. Brain Res. 2008, 193(2):311-314.
26. Mineur Y.M., Belzung C., Crusio W.E. Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behav. Brain Res. 2006, 175(1):43-50.
27. D'Aquila P.S., Brain P., Willner P. Effects of chronic mild stress on performance in behavioural tests relevant to anxiety and depression. Physiol. Behav. 1994, 56(5):861-867.
28. Greenwood B.N., Strong P.V., Fleshner M. Lesions of the basolateral amygdala reverse the long-lasting interference with shuttle box escape by uncontrollable stress. Behav. Brain Res. Jul. 2010, 211(1):71-76.
29. Pare D., Duvarci S. Amygdala microcircuits mediating fear expression and extinction. Curr. Opin. Neurobiol. Aug. 2012, 22(4):717-723.
30. Bravo-Rivera C., Roman-Ortiz C., Brignoni-Perez E., Sotres-Bayon F., Quirk G.J. Neural structures mediating expression and extinction of platform-mediated avoidance. J. Neurosci. Jul. 2014, 34(29):9736-9742.
31. Baker T.B., Piper M.E., McCarthy D.E., Majeskie M.R., Fiore M.C. Addiction motivation reformulated: an affective processing model of negative reinforcement. Psychol. Rev. Jan. 2004, 111(1):33-51.
32. Khantzian E.J. The self-medication hypothesis of addictive disorders: focus on heroin and cocaine dependence. Am. J. Psychiatry 1985, 142(11):1259-1264.
33. Koob G.F., Le Moal M. Drug abuse: hedonic homeostatic dysregulation. Science Oct. 1997, 278(5335):52-58. (80-).
34. Schaumberg K., Vinci C., Raiker J.S., Mota N., Jackson M., Whalen D., Schumacher J.A., Coffey S.F. PTSD-related alcohol expectancies and impulsivity interact to predict alcohol use severity in a substance dependent sample with PTSD. Addict. Behav. Sep. 2014, 41:41-45.
35. Cooper M.L., Russell M., Frone M.R. Work stress and alcohol effects: a test of stress-induced drinking. J. Health Soc. Behav. Sep. 1990, 31(3):260-276.
36. Finy M.S., Bresin K., Korol D.L., Verona E. Impulsivity, risk taking, and cortisol reactivity as a function of psychosocial stress and personality in adolescents. Dev. Psychopathol. Apr. 8 2014, 1-19.
37. James L.M., Strom T.Q., Leskela J. Risk-Taking Behaviors and Impulsivity Among Veterans With and Without PTSD and Mild TBI. Mil. Med. 2014, 179(4):357-363.
38. Johnson V., Pandina R.J. A longitudinal examination of the relationships among stress, coping strategies, and problems associated with alcohol use. Alcohol. Clin. Exp. Res. Jun. 1993, 17(3):696-702.
39. Sinha R., Jastreboff A.M. Stress as a common risk factor for obesity and addiction. Biol. Psychiatry May 2013, 73(9):827-835.
40. Arnsten A.F.T. Catecholamine influences on dorsolateral prefrontal cortical networks. Biol. Psychiatry June 2011, 69(12):e89-e99.
41. Arnsten A.F.T., Li B.M. Neurobiology of executive functions: catecholamine influences on prefrontal cortical functions. Biol. Psychiatry June 2005, 57(11):1377-1384.
42. 2-adrenoceptors in monkeys. NeuroReport 2003, 14(7):1013-1016.