Brief exposure to predator odor and resultant anxiety enhances mesocorticolimbic activity and enkephalin expression in CD-1 mice

European Journal of Neuroscience

Volumn 20, Issue 9, 2004, Pages 2415-2429

  Hebb, Andrea L O ^a   Zacharko, Robert M ^a   Gauthier, Michelle ^a   Trudel, France ^b   Laforest, Sylvie ^b   Drolet, Guy ^b  

^a CARLETON UNIVERSITY   (Canada)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

Accumbens; Amygdala; Butyric acid; Fos related antigen; Freezing

Indexed keywords

2,5 DIHYDRO 2,4,5 TRIMETHYLTHIAZOLINE; BUTYRIC ACID; ENKEPHALIN; MESSENGER RNA; SODIUM CHLORIDE; THIAZOLE DERIVATIVE; TRANSCRIPTION FACTOR FRA 1; TRANSCRIPTION FACTOR FRA 2; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; AVERSION; CELL COUNT; CONTROLLED STUDY; COPING BEHAVIOR; FEAR; FOX; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LIGHT DARK CYCLE; LIMBIC CORTEX; MALE; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; ODOR; PREDATOR; PRIORITY JOURNAL; STRESS; VENTRAL TEGMENTUM;

ADMINISTRATION, INHALATION; AMYGDALA; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CEREBRAL CORTEX; ENKEPHALINS; FEAR; LIMBIC SYSTEM; MALE; MICE; NEURAL PATHWAYS; NEURONS; NUCLEUS ACCUMBENS; ODORS; PROTO-ONCOGENE PROTEINS C-FOS; RNA, MESSENGER; SMELL; STRESS, PSYCHOLOGICAL; THIAZOLES; UP-REGULATION; VENTRAL TEGMENTAL AREA;

EID: 8144220169     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03704.x     Document Type: Article

References (87)

1. Agmo, A., Galvan, A., Heredia, A. & Morales, M. (1995) Naloxone blocks the antianxiety but not the motor effects of benzodiazepines and pentobarbital: experimental studies and literature review. Psychopharmacology (Berl.), 120, 186-194.
2. Andrews, N., Barnes, N.M., Steward, L.J., West, K.E., Cunningham, J., Wu, P.Y., Zangrossi, H. Jr & File, S.E. (1993) A comparison of rat brain amino acid and monoamine content in diazepam withdrawal and after exposure to a phobic stimulus. Br. J. Pharmacol., 109, 171-174.
3. Barrot, M., Marinelli, M., Abrous, D.N., Rouge-Pont, F., Le Moal, M. & Piazza, P.V. (1999) Functional heterogeneity in dopamine release and in the expression of Fos-like proteins within the rat striatal complex. Eur. J. Neurosci, 11, 1155-1166.
4. Bell, I.R., Schwanz, G.E., Bootzin, R.R., Hau, V. & Davis, T.P. (1997) Elevation of plasma beta-endorphin levels of shy elderly in response to novel laboratory experiences. Behav. Med., 22, 168-173.
5. Belzung, C. & Agmo, A. (1997) Naloxone blocks anxiolytic-like effects of benzodiazepines in Swiss but not in Balb/c mice. Psychopharmacology (Berl.), 132, 195-201.
6. Blanchard, D.C., Griebel, G. & Blanchard, R.J. (2001) Mouse defensive behaviors: pharmacological and behavioral assays for anxiety and panic. Neurosci. Biobehav. Rev., 25, 205-218.
7. Blanchard, D.C., Weatherspoon, A., Shepherd, J., Rodgers, R.J., Weiss, S.M. & Blanchard, R.J. (1991) 'Paradoxical' effects of morphine on antipredator defense reactions in wild and laboratory rats. Pharmacol. Biochem. Behav., 40, 819-828.
8. Blanchard, R.J., Blanchard, D.C., Rodgers, J. & Weiss, S.M. (1990) The characterization and modelling of antipredator defensive behavior. Neurosci. Biobehav. Rev., 14, 463-472.
9. Bohnen, N., Nicolson, N., Sulon, J. & Jolies, J. (1991) Coping style, trait anxiety and cortisol reactivity during mental stress. J. Psychosom. Res., 35, 141-147.
10. Breier, A. (1989) A.E. Bennett award paper. Experimental approaches to human stress research: assessment of neurobiological mechanisms of stress in volunteers and psychiatric patients. Biol. Psychiat., 26, 438-462.
11. Campeau, S., Falls, W.A., Cullinan, W.E., Helmreich, D.L., Davis, M. & Watson, S.J. (1997) Elicitation and reduction of fear: behavioural and neuroendocrine indices and brain induction of the immediate-early gene c-fos. Neuroscience, 78, 1087-1104.
12. Cohen, H., Zohar, J. & Matar, M. (2003) The relevance of differential response to trauma in an animal model of posttraumatic stress disorder. Biol. Psychiat., 53, 463-473.
13. Costall, B., Jones, B.J., Kelly, M.E., Naylor, R.J. & Tomkins, D.M. (1989) Exploration of mice in a black and white test box: validation as a model of anxiety. Pharmacol. Biochem. Behav., 32, 777-785.
14. Cui, X.J. & Vaillant, G.E. (1997) Does depression generate negative life events? J. Nerv. Ment. Dis., 185, 145-150.
15. Daunais. J.B., Letchworth, S.R., Sim-Selley, L.J., Smith, H.R., Childers, S.R. & Porrino, L.J. (2001) Functional and anatomical localization of mu opioid receptors in the striatum, amygdala, and extended amygdala of the nonhuman primate. J. Comp. Neurol., 433, 471-485.
16. Davis, M. (1998) Are different parts of the extended amygdala involved in fear versus anxiety? Biol. Psychiat., 44, 1239-1247.
17. Dielenberg, R.A., Hunt, G.E. & McGregor, I.S. (2001) 'When a rat smells a cat': the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience, 104, 1085-1097.
18. Dumont, E.G., Kinkead, R., Trottier, J., Gosselin, I. & Drolet, G. (2000) Effect of chronic psychogenic stress exposure on enkephalin neuronal activity and expression in the rat hypothalamic paraventricular nucleus. J. Neurochem., 75, 2200-2211.
19. Feldner, M.T., Zvolensky, M.J., Eifert, G.H. & Spira, A.P. (2003) Emotional avoidance: an experimental test of individual differences and response suppression using biological challenge. Behav. Res. Ther., 41, 403-411.
20. Fendt, M., Endres, T. & Apfelbach, R. (2003) 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., 23, 23-28.
21. Filliol, D., Ghozland, S., Chluba, J., Martin, M., Matthes, H.W. Simonin, F., Befort, K., Gaveriaux-Ruff, C., Dierich, A., LeMeur, M., Valverde, O., Maldonado, R. & Kieffer, B.L. (2000) Mice deficient for delta- and mu-opioid receptors exhibit opposing alterations of emotional responses. Nat. Genet., 25, 195-200.
22. Franklin, K.B. & Paxinos, G. (1996) The Mouse Brain in Stereotaxic Coordinates, 1st Edn. Academic Press, San Diego.
23. Funk, D. & Amir, S. (2000) Circadian modulation of fos responses to odor of the red fox, a rodent predator, in the rat olfactory system. Brain Res., 866, 262-267.
24. Goldstein, M.J. (1973) Individual differences in response to stress. Am. J. Commun. Psychol., 1, 113-137.
25. Goodwin, G.A. & Barr, G.A. (1997) Evidence for opioid and nonopioid processes mediating adaptive responses of infant rats that are repeatedly isolated. Dev. Psychobiol, 31, 217-227.
26. Guthrie, K.M. & Gall, C.M. (1995) Odors increase Fos in olfactory bulb neurons including dopaminergic cells. Neuroreport, 6, 2145-2149.
27. Haber, S.N., Kunishio, K., Mizobuchi, M. & Lynd-Balta, E. (1995) The orbital and medial prefrontal circuit through the primate basal ganglia. J. Neurosci., 15, 4851-4867.
28. Harro, J., Kiivet, R.A., Lang, A. & Vasar, E. (1990) Rats with anxious or non-anxious type of exploratory behaviour, differ in their brain CCK-8 and benzodiazepine receptor characteristics. Behav. Brain Res., 39, 63-71.
29. Hayley, S., Borowski, T., Merali, Z. & Anisman, H. (2001) Central monoamine activity in genetically distinct strains of mice following a psychogenic stressor: effects of predator exposure. Brain Res., 892, 293-300.
30. Hebb, A.L., Zacharko, R.M., Gauthier, M. & Drolet, G. (2003) Exposure of mice to a predator odor increases acoustic, startle but does not disrupt the rewarding properties of VTA intracranial self-stimulation. Brain Res., 982, 195-210.
31. Hebb, A.L.O., Mendella, P.D. & Zacharko, R.M. (1997) Immediate delta-receptor activation, following Stressor imposition influences behavioral reactivity to a subsequent stressful encounter. Soc. Neurosci. Abstr., 23, 1857.
32. Herrera, D.G. & Robertson, H.A. (1996) Activation of c-fos in the brain. Prog. Neurobiol., 50, 83-107.
33. Ho, Y.J., Eichendorff, J. & Schwarting, R.K. (2002) Individual response profiles of male Wistar rats in animal models for anxiety and depression. Behav. Brain Res., 136, 1-12.
34. Hogg, S. & File, S.E. (1994) Responders and nonresponders to cat odor do not differ in other tests of anxiety. Pharmacol. Biochem. Behav., 49, 219-222.
35. Hope, B.T., Kelz, M.B., Duman, R.S. & Nestler, E.J. (1994) Chronic electroconvulsive seizure (ECS) treatment results in expression of a long-lasting AP-1 complex in brain with altered composition and characteristics. J. Neurosci., 14, 4318-4328.
36. Hotsenpiller, G. & Williams, J.L. (1997) A synthetic predator odor (TMT) enhances conditioned analgesia and fear when paired with a benzodiazepine receptor inverse agonist (FG-7142). Psychobiology, 25, 83-88.
37. Houtman, I.L. & Bakker, F.C. (1991) Individual differences in reactivity to and coping with the stress of lecturing. J. Psychosom. Res., 35, 11-24.
38. Ibarra, P., Bruehl, S.P., McCubbin, J.A., Carlson, C.R., Wilson., J.F., Norton, J.A. & Montgomery, T.B. (1994) An unusual reaction to opioid blockade with naltrexone in a case of post-traumatic stress disorder. J. Trauma Stress, 7, 303-309.
39. Jamner, L.D. & Leigh, H. (1999) Repressive/defensive coping, endogenous opioids and health: how a life so perfect can make you sick. Psychiat. Res., 85, 17-31.
40. Johnson, P.I., Goodman, J.B., Condon, R. & Stellar, J.R. (1995) Reward shifts and motor responses following microinjections of opiate-specific agonists into either the core or shell of the nucleus accumbens. Psychopharmacology (Berl.), 120, 195-202.
41. Kabbaj. M., Devine, D., Savage, V. & Akil, H. (2000) Neurobiological correlates of individual differences in novelty-seeking behavior in the rat: Differential expression of stress-related molecules. J. Neurosci., 20, 6983-6988.
42. Kalin, N.H., Shelton, S.E. & Barksdale, C.M. (1988) Opiate modulation of separation-induced distress in non-human primates. Brain Res., 440. 285-292.
43. Kang, W., Wilson, S.P. & Wilson, M.A. (1999) Changes in nociceptive and anxiolytic responses following herpes virus-mediated preproenkephalin overexpression in rat amygdala are naloxone-reversible and transient. Ann. N.Y. Acad. Sci., 877, 751-755.
44. Kang, W., Wilson, S.P. & Wilson, M.A. (2000) Overexpression of proenkephalin in the amygdala potentiates the anxiolytic effects of benzociazepines. Neuropsychopharmacology. 22, 77-88.
45. Kavaliers, M. (1988) Brief exposure to a natural predator, the short-tailed weasel, induces benzodiazepine-sensitive analgesia in white-footed mice. Physiol. Behav., 43, 187-193.
46. Kavaliers. M. & Choleris, E. (2001) Antipredator responses and defensive behavior: ecological and ethological approaches for the neurosciences. Neurosci. Biobehav. Rev., 25, 577-586.
47. Kellner, M., Yassouridis, A., Hua, Y., Wendrich, M., Naber, D. & Wiedemann, K. (2002) Trait dissociation affects the behavioral response to cholecystokinn tetrapeptide in healthy man. Psychiat. Res., 111, 93-96.
48. Kemble, E. (1994) Novel odors increase defensiveness and inhibit attack behavior in mice. In Cooper. S. & Hendrie, C. (Eds), Ethology and Psychopharmacology. John Wiley, Chichester, pp. 191-204.
49. Kemble, E.D. & Bolwahnn, B.L. (1997) Immediate and long-term effects of novel odors ion risk assessment in mice. Physiol. Behav., 61, 543-549.
50. Kieffer, B.L. (1999) Opioids: first lessons from knockout mice. Trends Pharmacol. Sci., 20, 19-26.
51. Kollack-Walker, S. & Newman, S.W. (1995) Mating and agonistic behavior produce different patterns of Fos immunolabeling in the male Syrian hamster brain. Neuroscience, 66, 721-736.
52. Konig, M., Zimmer, A.M., Steiner, H., Hohnes, P.V., Crawley, J.N., Brownstein, M.J. & Zimmer, A. (1996) Pain responses, anxiety and aggression in mice deficient in pre-proenkephalin. Nature, 383, 535-538.
53. Lester, L.S. & Fanselow, M.S. (1985) Exposure to a cat produces opioid analgesia in rats. Behav. Neurosci., 99, 756-759.
54. Loas, G. (1996) Vulnerability to depression: a model centered on anhedonia. J. Affect. Disord., 41, 39-53.
55. MacNeil, G., Sela, Y., McIntosh, J. & Zacharko, R.M. (1997) Anxiogenic behavior in the light-dark paradigm following intraventricular administration of cholecystokinin-8S, restraint stress, or uncontrollable footshock in the CD-1 mouse. Pharmacol. Biochem. Behav., 58, 737-746.
56. Maremmani, I., Marini, G. & Fornai, F. (1998) Naltrexone-induced panic attacks. Am. J. Psychiat., 155, 447.
57. Mongeau, R., Miller, G.A., Chiang, E. & Anderson, D.J. (2003) Neural correlates of competing fear behaviors evoked by an innately aversive stimulus. J. Neurosci., 23, 3855-3868.
58. Morrow, B.A., Elsworth, J.D. & Roth, R.H. (2001) Prenatal exposure to cocaine reduces the number and enhances reactivity of A10 dopaminergic neurons to environmental stress. Synapse, 41, 337-344.
59. Morrow, B.A., Redmond, A.J., Roth, R.H. & Elsworth, J.D. (2000) The predator odor, TMT, displays a unique, stress-like pattern of dopaminergic and endocrinological activation in the rat. Brain Res., 864, 146-151.
60. Nieto. M.M., Wilson, J., Cupo, A., Roques, B.P. & Noble, F. (2002) Chronic morphine treatment modulates the extracellular levels of endogenous enkephalins in rat brain structures involved in opiate dependence: a microdialysis study. J. Neurosci., 22, 1034-1041.
61. Oakes, M.E. & Coover, G.D. (1997) Effects of small amygdala lesions on fear, but not aggression, in the rat. Physiol. Behav., 61, 45-55.
62. Olive. M.F., Koenig, H.N., Nannini, M.A. & Hodge, C.W. (2001) Stimulation of endorphin neurotransmission in the nucleus accumbens by ethanol, cocaine, and amphetamine. J. Neurosci., 21, RC184.
63. Petrovich, G.D., Scicli, A.P., Thompson, R.F. & Swanson, L.W. (2000) Associative fear conditioning of enkephalin mRNA levels in central amygdalar neurons. Behav. Neurosci., 114, 681-686.
64. Piazza, H.V., Rouge-Pont, F., Deminiere, J.M., Kharoubi, M., Le Moal, M. & Simon, H. (1991) Dopaminergic activity is reduced in the prefrontal cortex and increased in the nucleus accumbens of rats predisposed to develop amphetamine self-administration. Brain Res., 567, 169-174.
65. Pliakas, A.M., Carlson, R.R., Neve, R.L., Konradi. C., Nestler, E.J. & Carlezon, W.A. Jr (2001) Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J. Neurosci., 21, 7397-7403.
66. Ragnauth, A., Schuller, A., Morgan, M., Chan, J., Ogawa, S., Pintar, J., Bodnar, RJ. & Pfaff, D.W. (2001) Female preproenkephalin-knockout mice display altered emotional responses. Proc. Natl Acad. Sci. U.S.A., 98, 1958-1963.
67. Reynolds, S.M. & Berridge, K.C. (2002) Positive and negative motivation in nucleus accumbens shell: bivalent rostrocaudal gradients for GABA-elicited eating, taste 'liking'/'disliking' reactions, place preference/avoidance, and fear. J. Neurosci., 22, 7308-7320.
68. Risch, S.C. (1997) Recent advances in depression research: from stress to molecular biology and brain imaging. J. Clin. Psychiat., 58 (Suppl. 5), 3-6.
69. Roozendaal, B., Koolhaas, J.M. & Bohus, B. (1991) Attenuated cardiovascular, neuroendocrine, and behavioral responses after a single footshock in central amygdaloid lesioned male rats. Physiol. Behav., 50, 771-775.
70. Rosario, L.A. & Abercrombie, E.D. (1999) Individual differences in behavioral reactivity: correlation with stress-induced norepinephrine efflux in the hippocampus of Sprague-Dawley rats. Brain Res. Bull., 48, 595-602.
71. Rosen, J.B., Fanselow, M.S., Young, S.L., Sitcoske, M. & Maren, S. (1998) Immediate-early gene expression in the amygdala following footshock stress and contextual fear conditioning. Brain Res., 796, 132-142.
72. Schwarting, R.K., Thiel, C.M., Muller, C.P. & Huston, J.P. (1998) Relationship between anxiety and serotonin in the ventral striatum. Neuroreport, 9, 1025-1029.
73. Shepherd, J.K., Blanchard, D.C., Weiss, S.M., Rodgers, R.J. & Blanchard, R.J. (1992) Morphine attenuates antipredator ultrasonic vocalizations in mixed-sex rat colonies. Pharmacol. Biochem. Behav., 41, 551-558.
74. Simmons, D., Arriza, J. & Swanson, L. (1989) A complete protocol for in situ hybridization. J. Histotechnol., 12, 169-181.
75. Steimer, T. & Driscoll, P. (2003) Divergent stress responses and coping styles in psychogenetically selected Roman high-(RHA) and low-(RLA) avoidance rats: behavioural, neuroendocrine and developmental aspects. Stress, 6, 87-100.
76. Steimer. T., la Fleur, S. & Schulz, P.E. (1997) Neuroendocrine correlates of emotional reactivity and coping in male rats from the Roman high (RHA/Verh)- and low (RLA/Verh)-avoidance lines. Behav. Genet., 27, 503-512.
77. Tsuda, M., Suzuki, T., Misawa, M. & Nagase, H. (1996) Involvement of the opioid system in the anxiolytic effect of diazepam in mice. Eur. J. Pharmacol., 307, 7-14.
78. Uehara, T., Sakado, K., Sakado, M., Sato, T. & Someya, T. (1999) Relationship between stress coping and personality in patients with major depressive disorder. Psychother. Psychosom., 68, 26-30.
79. Vochteloo, J.D. & Koolhaas, J.M. (1987) Medial amygdala lesions in male rats reduce aggressive behavior: interference with experience. Physiol. Behav., 41, 99-102.
80. Walker, D.L. & Davis, M. (1997) Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J. Neurosci., 11, 9375-9383.
81. Wallace. K. & Rosen, J. (2000) Predator odor as an unconditioned fear stimulus in rats: Elicitation of freezing by trimethylthiazoline, a component of fox feces. Behav. Neurosci., 114, 912-922.
82. White, F.J. (1996) Synaptic regulation of mesocorticolimbic dopamine neurons. Annu. Rev. Neurosci., 19, 405-436.
83. Zacharko, R.M., Koszycki, D., Mendella, P.D. & Bradwejn, J. (1995) Behavioral, neurochemical, anatomical and electrophysiological correlates of panic disorder: multiple transmitter interaction and neuropeptide colocalization. Prog. Neurobiol., 47, 371-423.
84. Zacharko, R.M., Maddeaux, C., Hebb, A.L., Mendella, P.D. & Marsh, N.J. (1998) Vulnerability to stressor-induced disturbances in self-stimulation from the dorsal and ventral A10 area: differential effects of intraventricular D-Ala2-Met5-enkephalinamide, D-Ala2, N-Me-Phe4, Gly-O15-enkephalin, and D-Pen2, D-Pen5-enkephalin administration. Brain Res. Bull., 47, 237-248.
85. Zacharko, R.M., Zalcman, S., Macneil, G., Andrews, M., Mendella, P.D. & Anisman, H. (1997) Differential effects of immunologic challenge on self-stimulation from the nucleus accumbens and the substantia nigra. Pharmacol. Biochem. Behav., 58, 881-886.
86. Zahm, D.S., Williams, E.A., Latimer, M.P. & Winn, P. (2001) Ventral mesopontine projections of the caudomedial shell of the nucleus accumbens and extended amygdala in the rat: double dissociation by organization and development. J. Comp. Neurol., 436, 111-125.
87. Zangrossi, H. Jr & File, S.E. (1994) Habituation and generalization of phobic responses to cat odor. Brain Res. Bull., 33, 189-194.