Personality traits in rats predict vulnerability and resilience to developing stress-induced depression-like behaviors, HPA axis hyper-reactivity and brain changes in pERK1/2 activity

Psychoneuroendocrinology

Volumn 37, Issue 8, 2012, Pages 1209-1223

  Castro, Jorge E ^a   Diessler, Shanaz ^a   Varea, Emilio ^a   Márquez, Cristina ^a   Larsen, Marianne H ^a   Cordero, M Isabel ^a   Sandi, Carmen ^a  

^a EPFL   (Switzerland)

Author keywords

Anxiety; Corticosterone; Depression; ERK1 2; Exploration; Personality; Stress

Indexed keywords

CORTICOSTERONE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ACUTE STRESS; AMYGDALOID NUCLEUS; ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BODY WEIGHT; CHRONIC STRESS; CONTROLLED STUDY; COPING BEHAVIOR; DEPRESSION; EXPLORATORY BEHAVIOR; FORCED SWIMMING TEST; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; NONHUMAN; PERSONALITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SOCIAL BEHAVIOR; SOCIAL INTERACTION; STRESS; TASK PERFORMANCE;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; DEPRESSION; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PERSONALITY; PHOSPHORYLATION; PITUITARY-ADRENAL SYSTEM; RATS; RATS, SPRAGUE-DAWLEY; RESILIENCE, PSYCHOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84862328158     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2011.12.014     Document Type: Article

References (85)

1. Adler L., Wedekind D., Pilz J., Weniger G., Huether G. Endocrine correlates of personality traits: a comparison between emotionally stable and emotionally labile healthy young men. Neuropsychobiology 1997, 35:205-210.
2. Ball S.A. The validity of an alternative five-factor measure of personality in cocaine abusers. Psychol. Assess. 1995, 7:148-154.
3. Ball S.A., Schottenfeld R.S. A five-factor model of personality and addiction, psychiatric, and AIDS risk severity in pregnant and postpartum cocaine misusers. Subst. Use Misuse 1997, 32:25-41.
4. Ballenger J.C., Post R.M., Jimerson D.C., Lake C.R., Murphy D.L., Zuckerman M., Cronin C. Biochemical correlates of personality traits in normals: an exploratory study. Pers. Indiv. Differ. 1983, 4:615-625.
5. Bisaz R., Schachner M., Sandi C. Causal evidence for the involvement of the neural cell adhesion molecule, NCAM, in chronic stress-induced cognitive impairments. Hippocampus 2011, 21(1):56-71.
6. Botreau F., Gisquet-Verrier P. Memory reactivation, dissociated from behavioural expression, decreases ERK phosphorylation in the rat prefrontal cortex and amygdala. Behav. Brain Res. 2006, 169(1):176-180.
7. Bravo J.A., Díaz-Veliz G., Mora S., Ulloa J.L., Berthoud V.M., Morales P., Arancibia S., Fiedler J.L. Desipramine prevents stress-induced changes in depressive-like behavior and hippocampal markers of neuroprotection. Behav. Pharmacol. 2009, 20(3):273-285.
8. Castro J.E., Varea E., Márquez C., Cordero M.I., Poirier G., Sandi C. Role of the amygdala in antidepressant effects on hippocampal cell proliferation and survival and on depression-like behavior in the rat. PLoS One 2010, 5(1):e8618.
9. Cavigelli S.A., Stine M.M., Kovacsics C., Jefferson A., Diep M.N., Barrett C.E. Behavioral inhibition and glucocorticoid dynamics in a rodent model. Physiol. Behav. 2007, 92(5):897-905.
10. Conrad C.D., LeDoux J.E., Magariños A.M., McEwen B.S. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav. Neurosci. 1999, 113(5):902-913.
11. Cordero M.I., Rodríguez J.J., Davies H.A., Peddie C.J., Sandi C., Stewart M.G. Chronic restraint stress down-regulates amygdaloid expression of polysialylated neural cell adhesion molecule. Neuroscience 2005, 133(4):903-910.
12. Crawley J., Goodwin F.K. Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol. Biochem. Behav. 1980, 13(2):167-170.
13. de Kloet C.S., Vermetten E., Heijnen C.J., Geuze E., Lentjes E.G., Westenberg H.G. Enhanced cortisol suppression in response to dexamethasone administration in traumatized veterans with and without post-traumatic stress disorder. Psychoneuroendocrinology 2007, 32(3):215-226.
14. de Kloet E.R., Joëls M., Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
15. de Rijk R., de Kloet E.R. Corticosteroid receptor genetic polymorphisms and stress responsivity. Endocrine 2005, 28(3):263-270.
16. Doremus T.L., Varlinskaya E.I., Spear L.P. Factor analysis of elevated plus-maze behavior in adolescent and adult rats. Pharmacol. Biochem. Behav. 2006, 83:570-577.
17. Drevets W.C., Price J.L., Simpson J.R., Todd R.D., Reich T., Vannier M. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 1997, 386(6627):824-827.
18. Drugan R.C., Skolnick P., Paul S.M., Crawley J.N. A pretest procedure reliably predicts performance in two animal models of inescapable stress. Pharmacol. Biochem. Behav. 1989, 33(3):649-654.
19. Duclot F., Hollis F., Darcy M.J., Kabbaj M. Individual differences in novelty-seeking behavior in rats as a model for psychosocial stress-related mood disorders. Physiol. Behav. 2011, 104(2):296-305.
20. Feder A., Nestler E.J., Charney D.S. Psychobiology and molecular genetics of resilience. Nat. Rev. Neurosci. 2009, 10(6):446-457.
21. Fendt M., Endres T. 2,3,5-Trimethyl-3-thiazoline (TMT), a component of fox odor - just repugnant or really fear-inducing?. Neurosci. Biobehav. Rev. 2008, 32(7):1259-1266.
22. Fuss J., Ben Abdallah N.M., Vogt M.A., Touma C., Pacifici P.G., Palme R. Voluntary exercise induces anxiety-like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis. Hippocampus 2010, 20(3):364-376.
23. Grissom N.M., Bhatnagar S. The basolateral amygdala regulates adaptation to stress via β-adrenergic receptor-mediated reductions in phosphorylated extracellular signal-regulated kinase. Neuroscience 2011, 31(178):108-122.
24. Gunnar M.R., Tout K., De Haan M., Pierce S., Stansbury K. Temperament, social competence, and adrenocortical activity in preschoolers. Dev. Psychobiol. 1997, 31:65-85.
25. Gutièrrez-Mecinas M., Trollope A.F., Collins A., Morfett H., Hesketh S.A., Kersanté F., Reul J.M. Long-lasting behavioral responses to stress involve a direct interaction of glucocorticoid receptors with ERK1/2-MSK1-Elk-1 signaling. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(33):13806-13811.
26. Hennig J. Personality, serotonin, and noradrenaline. On the Psychobiology of Personality 2004, vol. 20:379-408. Elsevier B.V., Amsterdam.
27. Herrero A.I., Sandi C., Venero C. Individual differences in anxiety trait are related to spatial learning abilities and hippocampal expression of mineralocorticoid receptors. Neurobiol. Learn. Mem. 2006, 86(2):150-159.
28. Holmes A., Wellman C.L. Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci. Biobehav. Rev. 2009, 33(6):773-783.
29. Ilin Y., Richter-Levin G. Enriched environment experience overcomes learning deficits and depressive-like behavior induced by juvenile stress. PLoS One 2009, 4(1):e4329.
30. Jama A., Cecchi M., Calvo N., Watson S.J., Akil H. Inter-individual differences in novelty-seeking behavior in rats predict differential responses to desipramine in the forced swim test. Psychopharmacology (Berl) 2008, 198(3):333-340.
31. Kendler K.S., Gatz M., Gardner C.O., Pedersen N.L. Personality and major depression: a Swedish longitudinal, population-based twin study. Arch. Gen. Psychiatry 2006, 63(10):1113-1120.
32. Lara D.R., Akiskal H.S. Toward an integrative model of the spectrum of mood, behavioral and personality disorders based on fear and anger traits: II. Implications for neurobiology, genetics and psychopharmacological treatment. J. Affect. Disord. 2006, 94(1-3):89-103.
33. Larsen M.H., Mikkelsen J.D., Hay-Schmidt A., Sandi C. Regulation of brain-derived neurotrophic factor (BDNF) in the chronic unpredictable stress rat model and the effects of chronic antidepressant treatment. J. Psychiatr. Res. 2010, 44(13):808-816.
34. Lindfors P., Lundberg U. Is low cortisol release an indicator of positive health. Stress Health 2002, 18:153-160.
35. Lupien S.J., de Leon M., de Santi S., Convit A., Tarshish C., Nair N.P., et al. Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat. Neurosci. 1998, 1(1):69-73.
36. Magariños A.M., McEwen B.S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 1995, 69(1):83-88.
37. Marquez C., Nadal R., Armario A. The hypothalamic-pituitary-adrenal and glucose responses to daily repeated immobilisation stress in rats: individual differences. Neuroscience 2004, 123(3):601-612.
38. Mazur A. Biosocial models of deviant behavior among male army veterans. Biol. Psychol. 1995, 41:271-293.
39. Mazzucchelli C., Brambilla R. Ras-related and MAPK signalling in neuronal plasticity and memory formation. Cell. Mol. Life Sci. 2000, 57(4):604-611.
40. McEwen B.S. Effects of adverse experiences for brain structure and function. Biol. Psychiatry 2000, 48(8):721-731.
41. McEwen B.S. Early life influences on life-long patterns of behavior and health. Ment. Retard. Dev. Disabil. Res. Rev. 2003, 9(3):149-154.
42. McEwen B.S. Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann. N. Y. Acad. Sci. 2004, 1032:1-7.
43. Minor T.R., Dess N.K., Ben-David E., Chang W.-C. Individual differences in vulnerability to inescapable shock in rats. J. Exp. Psychol. Anim. Behav. Process. 1994, 20(4):402-412.
44. Mitra R., Ferguson D., Sapolsky R.M. SK2 potassium channel overexpression in basolateral amygdala reduces anxiety, stress-induced corticosterone secretion and dendritic arborization. Mol. Psychiatry 2009, 14(9):847-855. 827.
45. Mitra R., Jadhav S., McEwen B.S., Vyas A., Chattarji S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(26):9371-9376.
46. Mitra R., Sapolsky R.M. Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(14):5573-5578.
47. New A.S., Fan J., Murrough J.W., Liu X., Liebman R.E., Guise K.G., Tang C.Y., Charney D.S. A functional magnetic resonance imaging study of deliberate emotion regulation in resilience and posttraumatic stress disorder. Biol. Psychiatry 2009, 66(7):656-664.
48. Oitzl M.S., Champagne D.L., van der Veen R., de Kloet E.R. Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci. Biobehav. Rev. 2010, 34(6):853-856.
49. Oitzl M.S., Workel J.O., Fluttert M., Frosch F., de Kloet E.R. Maternal deprivation affects behaviour from youth to senescence: amplification of individual differences in spatial learning and memory in senescent Brown Norway rats. Eur. J. Neurosci. 2000, 12(10):3771-3780.
50. Pham K., Nacher J., Hof P.R., McEwen B.S. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 2003, 17(4):879-886.
51. Piazza P.V., Deminiere J.M., Le Moal M., Simon H. Factors that predict individual vulnerability to amphetamine self-administration. Science 1989, 245(4925):1511-1513.
52. Pickering A.D. The neuropsychology of impulsive antisocial sensation seeking personality traits: from dopamine to hippocampal function?. On the Psychobiology of Personality 2004, vol. 23:459-476. Elsevier B.V., Amsterdam.
53. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266(5604):730-732.
54. Qi X., Lin W., Li J., Pan Y., Wang W. The depressive-like behaviors are correlated with decreased phosphorylation of mitogen-activated protein kinases in rat brain following chronic forced swim stress. Behav. Brain Res. 2006, 175:233-240.
55. Rajkowska G. Histopathology of the prefrontal cortex in major depression: what does it tell us about dysfunctional monoaminergic circuits?. Prog. Brain Res. 2000, 126:397-412.
56. Refojo D., Echenique C., Muller M.B., Reul J.M., Deussing J.M., Wurst W., Sillaber I., Paez-Pereda M., Holsboer F., Arzt E. Corticotropin-releasing hormone activates ERK1/2 MAPK in specific brain areas. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:6183-6188.
57. Renthal W., Maze I., Krishnan V., Covington H.E., Xiao G., Kumar A., et al. Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 2007, 56(3):517-529.
58. Reul J.M., Chandramohan Y. Epigenetic mechanisms in stress-related memory formation. Psychoneuroendocrinology 2007, 32(Suppl. 1):S21-S25.
59. Revest J.M., Dupret D., Koehl M., Funk-Reiter C., Grosjean N., Piazza P.V., et al. Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol. Psychiatry 2009, 14:959-967.
60. Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nat. Rev. Neurosci. 2009, 10:423-433.
61. Rosenblitt J.C., Soler H., Johnson S.E., Quadagno D.M. Sensation seeking and hormones in men and women: exploring the link. Horm. Behav. 2001, 40:396-402.
62. Rotllant D., Márquez C., Nadal R., Armario A. The brain pattern of c-fos induction by two doses of amphetamine suggests different brain processing pathways and minor contribution of behavioural traits. Neuroscience 2010, 168(3):691-705.
63. Rudolph K.D., Hammen C. Age and gender as determinants of stress exposure, generation, and reactions in youngsters: a transactional perspective. Child Dev. 1999, 70(3):660-677.
64. Salehi B., Cordero M.I., Sandi C. Learning under stress: the inverted-U-shape function revisited. Learn. Mem. 2010, 17(10):522-530.
65. Sandi C., Cordero M.I., Ugolini A., Varea E., Caberlotto L., et al. Chronic stress-induced alterations in amygdala responsiveness and behavior-modulation by trait anxiety and corticotropin-releasing factor systems. Eur. J. Neurosci. 2008, 28:1836-1848.
66. Sandi C., Richter-Levin G. From high anxiety trait to depression: a neurocognitive hypothesis. Trends Neurosci. 2009, 32:312-320.
67. Sheline Y.I., Sanghavi M., Mintun M.A., Gado M.H. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J. Neurosci. 1999, 19(12):5034-5043.
68. Shen C.P., Tsimberg Y., Salvadore C., Meller E. Activation of Erk and JNK MAPK pathways by acute swim stress in rat brain regions. BMC Neurosci. 2004, 5:36.
69. Silberstein S., Vogl A.M., Refojo D., Senin S.A., Wurst W., Holsboer F., Deussing J.M., Arzt E. Amygdaloid pERK1/2 in corticotropin-releasing hormone overexpressing mice under basal and acute stress conditions. Neuroscience 2009, 159:610-617.
70. Southwick S.M., Vythilingam M., Charney D.S. The psychobiology of depression and resilience to stress: implications for prevention and treatment. Annu. Rev. Clin. Psychol. 2005, 1:255-291.
71. Stam R. PTSD and stress sensitisation: a tale of brain and body Part 2: animal models. Neurosci. Biobehav. Rev. 2007, 31(4):558-584.
72. Stiller A.L., Drugan R.C., Hazi A., Kent S.P. Stress resilience and vulnerability: the association with rearing conditions, endocrine function, immunology, and anxious behavior. Psychoneuroendocrinology 2011, 36(9):1383-1395.
73. Todorovic C., Sherrin T., Pitts M., Hippel C., Rayner M., Spiess J. Suppression of the MEK/ERK signaling pathway reverses depression-like behaviors of CRF2-deficient mice. Neuropsychopharmacology 2009, 34(6):1416-1426.
74. Tyrka A.R., Wier L.M., Price L.H., Rikhye K., Ross N.S., Anderson G.M., Wilkinson C.W., Carpenter L.L. Cortisol and ACTH responses to the Dex/CRH test: influence of temperament. Horm. Behav. 2008, 53(4):518-525.
75. Vyas A., Jadhav S., Chattarji S. Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala. Neuroscience 2006, 143(2):387-393.
76. Vyas A., Mitra R., ShankaranarayanaRao B.S., Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J. Neurosci. 2002, 22(15):6810-6818.
77. Vyas A., Pillai A.G., Chattarji S. Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 2004, 128(4):667-673.
78. Walker F.R., Masters L.M., Dielenberg R.A., Day T.A. Coping with defeat: acute glucocorticoid and forebrain responses to social defeat vary with defeat episode behaviour. Neuroscience 2009, 162(2):244-253.
79. Walker F.R., Hinwood M., Masters L., Deilenberg R.A., Day T.A. Individual differences predict susceptibility to conditioned fear arising from psychosocial trauma. J. Psychiatr. Res. 2008, 42(5):371-383.
80. Wang W., Du W., Lieu P., Lieu J., Wang Y. Five-factor measures in Chinese university students: effects of one-child policy?. Psychiatry Res. 2002, 109:37-44.
81. Wang W., Du W., Wang Y., Livesley W.J., Jang K.L. The relationship between the Zuckerman-Kuhlman Personality Questionnaire and traits delineating personality pathology. Pers. Indiv. Differ. 2004, 36:155-162.
82. Willner P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 2005, 52(2):90-110.
83. Willner P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl) 1997, 134:319-329.
84. Wu S.L., Hsu L.S., Tu W.T., Wang W.F., Huang Y.T., Pawlak C.R., Ho Y.J. Effects of d-cycloserine on the behavior and ERK activity in the amygdala: role of individual anxiety levels. Behav. Brain Res. 2008, 187:246-253.
85. Yang R.J., Mozhui K., Karlsson R.M., Cameron H.A., Williams R.W., et al. Variation in mouse basolateral amygdala volume is associated with differences in stress reactivity and fear learning. Neuropsychopharmacology 2008, 33:2595-2604.