Sex differences in the behavioural and hypothalamic-pituitary-adrenal response to contextual fear conditioning in rats

Hormones and Behavior

Volumn 66, Issue 5, 2014, Pages 713-723

  Daviu, Núria ^a   Andero, Raül ^a   Armario, Antonio ^a   Nadal, Roser ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

ACTH; Anxiety; Corticosterone; Fear generalization; Freezing; HPA axis; Sex differences

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; COMPARATIVE STUDY; CONDITIONING; CONTROLLED STUDY; FEAR; FEMALE; FOOTSHOCK; HORMONE ACTION; HORMONE RESPONSE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LEARNING; MALE; NONHUMAN; RAT; REINFORCEMENT; SENSITIZATION; SEX DIFFERENCE; ANIMAL; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; METABOLISM; PHYSIOLOGY; SEXUAL DEVELOPMENT; WISTAR RAT;

ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); CORTICOSTERONE; CUES; FEAR; FEMALE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; PITUITARY-ADRENAL SYSTEM; RATS; RATS, WISTAR; SEX CHARACTERISTICS;

EID: 84908341385     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2014.09.015     Document Type: Article

References (88)

1. Albrecht A., Caliskan G., Oitzl M.S., Heinemann U., Stork O. Long-lasting increase of corticosterone after fear memory reactivation: anxiolytic effects and network activity modulation in the ventral hippocampus. Neuropsychopharmacology 2013, 38:386-394.
2. Aloisi A.M., Steenbergen H.L., van de Poll N.E., Farabollini F. Sex-dependent effects of restraint on nociception and pituitary-adrenal hormones in the rat. Physiol. Behav. 1994, 55:789-793.
3. Anagnostaras S.G., Maren S., DeCola J.P., Lane N.I., Gale G.D., Schlinger B.A., Fanselow M.S. Testicular hormones do not regulate sexually dimorphic Pavlovian fear conditioning or perforant-path long-term potentiation in adult male rats. Behav. Brain Res. 1998, 92:1-9.
4. Andero R., Daviu N., Escorihuela R.M., Nadal R., Armario A. 7,8-Dihydroxyflavone, a TrkB receptor agonist, blocks long-term spatial memory impairment caused by immobilization stress in rats. Hippocampus 2012, 22:399-408.
5. Armario A., Nadal R. Individual differences and the characterization of animal models of psychopathology: a strong challenge and a good opportunity. Front. Pharmacol. 2013, 4:137.
6. Armario A., Gavaldà A., Martí J. Comparison of the behavioural and endocrine response to forced swimming stress in five inbred strains of rats. Psychoneuroendocrinology 1995, 20:879-890.
7. Armario A., Escorihuela R.M., Nadal R. Long-term neuroendocrine and behavioural effects of a single exposure to stress in adult animals. Neurosci. Biobehav. Rev. 2008, 32:1121-1135.
8. Armario A., Daviu N., Muñoz-Abellán C., Rabasa C., Fuentes S., Belda X., Gagliano H., Nadal R. What can we know from pituitary-adrenal hormones about the nature and consequences of exposure to emotional stressors?. Cell. Mol. Neurobiol. 2012, 32:749-758.
9. Atkinson H.C., Waddell B.J. Circadian variation in basal plasma corticosterone and adrenocorticotropin in the rat: sexual dimorphism and changes across the estrous cycle. Endocrinology 1997, 138:3842-3848.
10. Babb J.A., Masini C.V., Day H.E., Campeau S. Stressor-specific effects of sex on HPA axis hormones and activation of stress-related neurocircuitry. Stress 2013, 16:664-677.
11. Babb J.A., Masini C.V., Day H.E., Campeau S. Sex differences in activated corticotropin-releasing factor neurons within stress-related neurocircuitry and hypothalamic-pituitary-adrenocortical axis hormones following restraint in rats. Neuroscience 2013, 234:40-52.
12. Baldi E., Lorenzini C.A., Bucherelli C. Footshock intensity and generalization in contextual and auditory-cued fear conditioning in the rat. Neurobiol. Learn. Mem. 2004, 81:162-166.
13. Barker J.M., Galea L.A. Males show stronger contextual fear conditioning than females after context pre-exposure. Physiol. Behav. 2010, 99:82-90.
14. Basso A.M., Gallagher K.B., Mikusa J.P., Rueter L.E. Vogel conflict test: sex differences and pharmacological validation of the model. Behav. Brain Res. 2011, 218:174-183.
15. Beatty W.W., Beatty P.A. Hormonal determinants of sex differences in avoidance behavior and reactivity to electric shock in the rat. J. Comp. Physiol. Psychol. 1970, 73:446-455.
16. Belda X., Márquez C., Armario A. Long-term effects of a single exposure to stress in adult rats on behavior and hypothalamic-pituitary-adrenal responsiveness: comparison of two outbred rat strains. Behav. Brain Res. 2004, 154:399-408.
17. Belda X., Fuentes S., Nadal R., Armario A. A single exposure to immobilization causes long-lasting pituitary-adrenal and behavioral sensitization to mild stressors. Horm. Behav. 2008, 54:654-661.
18. Belda X., Daviu N., Nadal R., Armario A. Acute stress induced sensitization of the pituitary-adrenal response to heterotypic stressors: independence of glucocorticoid release and activation of CRH1 receptors. Horm. Behav. 2012, 62:515-524.
19. Blanchard R.J., Blanchard D.C. Passive and active reactions to fear-eliciting stimuli. J. Comp. Physiol. Psychol. 1969, 68:129-135.
20. Bruijnzeel A.W., Stam R., Wiegant V.M. Effect of a benzodiazepine receptor agonist and corticotropin-releasing hormone receptor antagonists on long-term foot-shock-induced increase in defensive withdrawal behavior. Psychopharmacology 2001, 158:132-139.
21. Bruijnzeel A.W., Stam R., Wiegant V.M. LY354740 attenuates the expression of long-term behavioral sensitization induced by a single session of foot shocks. Eur. J. Pharmacol. 2001, 426:77-80.
22. Brunzell D.H., Coy A.E., Ayres J.J., Meyer J.S. Prenatal cocaine effects on fear conditioning: exaggeration of sex-dependent context extinction. Neurotoxicol. Teratol. 2002, 24:161-172.
23. Bucci D.J., Chiba A.A., Gallagher M. Spatial learning in male and female Long-Evans rats. Behav. Neurosci. 1995, 109:180-183.
24. Canli T., Desmond J.E., Zhao Z., Gabrieli J.D. Sex differences in the neural basis of emotional memories. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10789-10794.
25. Carr R., Bertasi F., Betancourt A., Bowers S., Gandy B.S., Ryan P., Willard S. Effect of neonatal rat bisphenol a exposure on performance in the Morris water maze. J. Toxicol. Environ. Health A 2003, 66:2077-2088.
26. Chang Y.J., Yang C.H., Liang Y.C., Yeh C.M., Huang C.C., Hsu K.S. Estrogen modulates sexually dimorphic contextual fear extinction in rats through estrogen receptor beta. Hippocampus 2009, 19:1142-1150.
27. Cook C.D., Moore K.I. Effects of sex, hindpaw injection site and stimulus modality on nociceptive sensitivity in arthritic rats. Physiol. Behav. 2006, 87:552-562.
28. Dalla C., Shors T.J. Sex differences in learning processes of classical and operant conditioning. Physiol. Behav. 2009, 97:229-238.
29. Daviu N., Fuentes S., Nadal R., Armario A. A single footshock causes long-lasting hypoactivity in unknown environments that is dependent on the development of contextual fear conditioning. Neurobiol. Learn. Mem. 2010, 94:183-190.
30. Daviu N., Delgado-Morales R., Nadal R., Armario A. Not all stressors are equal: behavioral and endocrine evidence for development of contextual fear conditioning after a single session of footshocks but not of immobilization. Front. Behav. Neurosci. 2012, 6:69.
31. Droste S.K., de Groote L., Lightman S.L., Reul J.M., Linthorst A.C. The ultradian and circadian rhythms of free corticosterone in the brain are not affected by gender: an in vivo microdialysis study in Wistar rats. J. Neuroendocrinol. 2009, 21:132-140.
32. Engeland W.C., Miller P., Gann D.S. Dissociation between changes in plasma bioactive and immunoreactive adrenocorticotropin after hemorrhage in awake dogs. Endocrinology 1989, 124:2978-2985.
33. Erskine M.S., Stern J.M., Levine S. Effects of prepubertal handling on shock-induced fighting and ACTH in male and female rats. Physiol. Behav. 1975, 14:413-420.
34. Faraday M.M., Blakeman K.H., Grunberg N.E. Strain and sex alter effects of stress and nicotine on feeding, body weight, and HPA axis hormones. Pharmacol. Biochem. Behav. 2005, 80:577-589.
35. Fendt M., Fanselow M.S. The neuroanatomical and neurochemical basis of conditioned fear. Neurosci. Biobehav. Rev. 1999, 23:743-760.
36. Frankland P.W., Cestari V., Filipkowski R.K., McDonald R.J., Silva A.J. The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav. Neurosci. 1998, 112:863-874.
37. Fredrikson M., Hugdahl K., Ohman A. Electrodermal conditioning to potentially phobic stimuli in male and female subjects. Biol. Psychol. 1976, 4:305-314.
38. Fuentes S., Daviu N., Gagliano H., Garrido P., Zelena D., Monasterio N., Armario A., Nadal R. Sex-dependent effects of an early life treatment in rats that increases maternal care: vulnerability or resilience?. Front. Behav. Neurosci. 2014, 8:56.
39. Gagliano H., Fuentes S., Nadal R., Armario a Previous exposure to immobilisation and repeated exposure to a novel environment demonstrate a marked dissociation between behavioral and pituitary-adrenal responses. Behav. Brain Res. 2008, 187:239-245.
40. Gala R.R., Westphal U. Corticosteroid-binding globulin in the rat: studies on the sex difference. Endocrinology 1965, 77:841-851.
41. Galea L.A., McEwen B.S., Tanapat P., Deak T., Spencer R.L., Dhabhar F.S. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 1997, 81:689-697.
42. González F., Quinn J.J., Fanselow M.S. Differential effects of adding and removing components of a context on the generalization of conditional freezing. J. Exp. Psychol. Anim. Behav. Process. 2003, 29:78-83.
43. Gresack J.E., Schafe G.E., Orr P.T., Frick K.M. Sex differences in contextual fear conditioning are associated with differential ventral hippocampal extracellular signal-regulated kinase activation. Neuroscience 2009, 159:451-467.
44. Hardin J.M., Hilbe J.M. Generalized Estimating Equations 2003, Champan and Hall/ CRC, Boca Raton.
45. Houston F.P., Stevenson G.D., McNaughton B.L., Barnes C.A. Effects of age on the generalization and incubation of memory in the F344 rat. Learn. Mem. 1999, 6:111-119.
46. Iwasaki-Sekino A., Mano-Otagiri A., Ohata H., Yamauchi N., Shibasaki T. Gender differences in corticotropin and corticosterone secretion and corticotropin-releasing factor mRNA expression in the paraventricular nucleus of the hypothalamus and the central nucleus of the amygdala in response to footshock stress or psychological stress in rats. Psychoneuroendocrinology 2009, 34:226-237.
47. Kissinger S.C., Riccio D.C. Stimulus conditions influencing the development of tolerance to repeated cold exposure in rats. Anim. Learn. Behav. 1995, 23:9-16.
48. Kudielka B.M., Kirschbaum C. Sex differences in HPA axis responses to stress: a review. Biol. Psychol. 2005, 69:113-132.
49. Laxmi T.R., Stork O., Pape H.C. Generalisation of conditioned fear and its behavioural expression in mice. Behav. Brain Res. 2003, 145:89-98.
50. Lebron-Milad K., Milad M.R. Sex differences, gonadal hormones and the fear extinction network: implications for anxiety disorders. Biol. Mood Anxiety Disord. 2012, 2:3.
51. LeDoux J. The emotional brain, fear, and the amygdala. Cell. Mol. Neurobiol. 2003, 23:727-738.
52. Li L., Fan X., Warner M., Xu X.J., Gustafsson J.A., Wiesenfeld-Hallin Z. Ablation of estrogen receptor alpha or beta eliminates sex differences in mechanical pain threshold in normal and inflamed mice. Pain 2009, 143:37-40.
53. Maren S. Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats. Eur. J. Neurosci. 2008, 28:1661-1666.
54. McCulloch C., Searle S. Generalized, Linear and Mixed Models 2001, Wiley and Sons, New York.
55. Merino J.J., Cordero M.I., Sandi C. Regulation of hippocampal cell adhesion molecules NCAM and L1 by contextual fear conditioning is dependent upon time and stressor intensity. Eur. J. Neurosci. 2000, 12:3283-3290.
56. Milad M.R., Zeidan M.A., Contero A., Pitman R.K., Klibanski A., Rauch S.L., Goldstein J.M. The influence of gonadal hormones on conditioned fear extinction in healthy humans. Neuroscience 2010, 168:652-658.
57. Muñoz-Abellán C., Andero R., Nadal R., Armario a Marked dissociation between hypothalamic-pituitary-adrenal activation and long-term behavioral effects in rats exposed to immobilization or cat odor. Psychoneuroendocrinology 2008, 33:1139-1150.
58. Muñoz-Abellán C., Daviu N., Rabasa C., Nadal R., Armario A. Cat odor causes long-lasting contextual fear conditioning and increased pituitary-adrenal activation, without modifying anxiety. Horm. Behav. 2009, 56:465-471.
59. Pamplona F.A., Henes K., Micale V., Mauch C.P., Takahashi R.N., Wotjak C.T. Prolonged fear incubation leads to generalized avoidance behavior in mice. J. Psychiatr. Res. 2011, 45:354-360.
60. Patchev V.K., Hayashi S., Orikasa C., Almeida O.F. Ontogeny of gender-specific responsiveness to stress and glucocorticoids in the rat and its determination by the neonatal gonadal steroid environment. Stress 1999, 3:41-54.
61. Peña Y., Prunell M., Rotllant D., Armario A., Escorihuela R.M. Enduring effects of environmental enrichment from weaning to adulthood on pituitary-adrenal function, pre-pulse inhibition and learning in male and female rats. Psychoneuroendocrinology 2009, 34:1390-1404.
62. Perrot-Sinal T.S., Kostenuik M.A., Ossenkopp K.P., Kavaliers M. Sex differences in performance in the Morris water maze and the effects of initial nonstationary hidden platform training. Behav. Neurosci. 1996, 110:1309-1320.
63. Pijlman F.T., van Ree J.M. Physical but not emotional stress induces a delay in behavioural coping responses in rats. Behav. Brain Res. 2002, 136:365-373.
64. Pijlman F.T., Herremans A.H., van de Kieft J., Kruse C.G., van Ree J.M. Behavioural changes after different stress paradigms: prepulse inhibition increased after physical, but not emotional stress. Eur. Neuropsychopharmacol. 2003, 13:369-380.
65. Radulovic J., Kammermeier J., Spiess J. Generalization of fear responses in C57BL/6N mice subjected to one-trial foreground contextual fear conditioning. Behav. Brain Res. 1998, 95:179-189.
66. Rhodes M.E., Rubin R.T. Functional sex differences ('sexual diergism') of central nervous system cholinergic systems, vasopressin, and hypothalamic-pituitary-adrenal axis activity in mammals: a selective review. Brain Res. Brain Res. Rev. 1999, 30:135-152.
67. Rhodes M.E., Balestreire E.M., Czambel R.K., Rubin R.T. Estrous cycle influences on sexual diergism of HPA axis responses to cholinergic stimulation in rats. Brain Res. Bull. 2002, 59:217-225.
68. Rivier C. Gender, sex steroids, corticotropin-releasing factor, nitric oxide, and the HPA response to stress. Pharmacol. Biochem. Behav. 1999, 64:739-751.
69. Roof R.L., Stein D.G. Gender differences in Morris water maze performance depend on task parameters. Physiol. Behav. 1999, 68:81-86.
70. Schell A.M., Dawson M.E., Marinkovic K. Effects of potentially phobic conditioned stimuli on retention, reconditioning, and extinction of the conditioned skin conductance response. Psychophysiology 1991, 28:140-153.
71. Seale J.V., Wood S.A., Atkinson H.C., Bate E., Lightman S.L., Ingram C.D., Jessop D.S., Harbuz M.S. Gonadectomy reverses the sexually diergic patterns of circadian and stress-induced hypothalamic-pituitary-adrenal axis activity in male and female rats. J. Neuroendocrinol. 2004, 16:516-524.
72. Seale J.V., Wood S.A., Atkinson H.C., Harbuz M.S., Lightman S.L. Gonadal steroid replacement reverses gonadectomy-induced changes in the corticosterone pulse profile and stress-induced hypothalamic-pituitary-adrenal axis activity of male and female rats. J. Neuroendocrinol. 2004, 16:989-998.
73. Siegmund A., Wotjak C.T. A mouse model of posttraumatic stress disorder that distinguishes between conditioned and sensitised fear. J. Psychiatr. Res. 2007, 41:848-860.
74. Silva-Gómez A.B., Bermudez M., Quirion R., Srivastava L.K., Picazo O., Flores G. Comparative behavioral changes between male and female postpubertal rats following neonatal excitotoxic lesions of the ventral hippocampus. Brain Res. 2003, 973:285-292.
75. Spinedi E., Salas M., Chisari A., Perone M., Carino M., Gaillard R.C. Sex differences in the hypothalamo-pituitary-adrenal axis response to inflammatory and neuroendocrine stressors. Evidence for a pituitary defect in the autoimmune disease-susceptible female Lewis rat. Neuroendocrinology 1994, 60:609-617.
76. Toufexis D.J., Myers K.M., Davis M. The effect of gonadal hormones and gender on anxiety and emotional learning. Horm. Behav. 2006, 50:539-549.
77. Vahl T.P., Ulrich-Lai Y.M., Ostrander M.M., Dolgas C.M., Elfers E.E., Seeley R.J., D'Alessio D.A., Herman J.P. Comparative analysis of ACTH and corticosterone sampling methods in rats. Am. J. Physiol. Endocrinol. Metab. 2005, 289:E823-E828.
78. Van den Berg C.L., Lamberts R.R., Wolterink G., Wiegant V.M., Van Ree J.M. Emotional and footshock stimuli induce differential long-lasting behavioural effects in rats; involvement of opioids. Brain Res. 1998, 799:6-15.
79. Van der Kar L.D., Piechowski R.A., Rittenhause P., Gray T.S. Amygdaloid lesions: differential effect on conditioned stress and immobilization-induced increases in corticosterone and renin secretion. Neuroendocronology 1991, 54:89-95.
80. Van Dijken H.H., Mos J., van der Heyden J.A., Tilders F.J. Characterization of stress-induced long-term behavioural changes in rats: evidence in favor of anxiety. Physiol. Behav. 1992, 52:945-951.
81. Van Dijken H.H., Tilders F.J., Olivier B., Mos J. Effects of anxiolytic and antidepressant drugs on long-lasting behavioural deficits resulting from one short stress experience in male rats. Psychopharmacology 1992, 109:395-402.
82. Van Dijken H.H., Van der Heyden J.A., Mos J., Tilders F.J. Inescapable footshocks induce progressive and long-lasting behavioural changes in male rats. Physiol. Behav. 1992, 51:787-794.
83. Viau V., Meaney M.J. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991, 129:2503-2511.
84. Wagner A.K., Willard L.A., Kline A.E., Wenger M.K., Bolinger B.D., Ren D., Zafonte R.D., Dixon C.E. Evaluation of estrous cycle stage and gender on behavioral outcome after experimental traumatic brain injury. Brain Res. 2004, 998:113-121.
85. Wang R.H., Bejar C., Weinstock M. Gender differences in the effect of rivastigmine on brain cholinesterase activity and cognitive function in rats. Neuropharmacology 2000, 39:497-506.
86. Watanobe H. Sexual dimorphism in the pituitary-adrenal response to tumor necrosis factor-alpha, but not to interleukin-6, in the rat. Brain Res. Bull. 2002, 57:151-155.
87. Wiltgen B.J., Silva A.J. Memory for context becomes less specific with time. Learn. Mem. 2007, 14:313-317.
88. Zelena D., Mergl Z., Foldes A., Kovacs K.J., Toth Z., Makara G.B. Role of hypothalamic inputs in maintaining pituitary-adrenal responsiveness in repeated restraint. Am. J. Physiol. Endocrinol. Metab. 2003, 285:E1110-E1117.