Coping style and stress hormone responses in genetically heterogeneous rats: Comparison with the Roman rat strains

Behavioural Brain Research

Volumn 228, Issue 1, 2012, Pages 203-210

  Díaz Morán, Sira ^a   Palència, Marta ^a   Mont Cardona, Carme ^a   Cañete, Toni ^a   Blázquez, Gloria ^a   Martínez Membrives, Esther ^a   López Aumatell, Regina ^b   Tobeña, Adolf ^a   Fernández Teruel, Alberto ^a  

^a INSTITUT DE NEUROCIÈNCIES   (Spain)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Anxiety; Behavioral hormonal associations; Fear; Genetically heterogeneous rats; Hypothalamus pituitary adrenal responses; Roman rat strains

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN; PROLACTIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; COPING BEHAVIOR; DEPRESSION; FEAR; FORCED SWIMMING TEST; GENETICALLY HETEROGENEOUS RAT; HORMONE RESPONSE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; ROMAN RAT; STRAIN DIFFERENCE;

ADAPTATION, PSYCHOLOGICAL; ADRENOCORTICOTROPIC HORMONE; ANIMALS; AVOIDANCE LEARNING; CORTICOSTERONE; EXPLORATORY BEHAVIOR; GENETIC HETEROGENEITY; IMMOBILITY RESPONSE, TONIC; MALE; MAZE LEARNING; PROLACTIN; RATS; RATS, INBRED STRAINS; SPECIES SPECIFICITY; STRESS, PSYCHOLOGICAL;

EID: 84855221083     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.12.002     Document Type: Article

References (66)

1. Aguilar R., Gil L., Flint J., Gray J.A., Dawson G.R., Driscoll P., et al. Learned fear, emotional reactivity and fear of heights: a factor analytic map from a large F2 intercross of Roman rat strains. Brain Res Bull 2002, 57:17-26.
2. Alam I., Koller D.L., Sun Q., Roeder R.K., Cañete T., Blázquez G., et al. Heterogeneous stock rat: a unique animal model for mapping genes influencing bone fragility. Bone 2011, 48:1169-1177.
3. Armario A., Escorihuela R.M., Nadal R. Long-term neuroendocrine and behavioural effects of a single exposure to stress in adult animal. Neurosci Biobehav Rev 2008, 32:1121-1135.
4. Armario A., Martí J. Forced swimming behaviour is not related to the corticosterone levels achieved in the test: a study with four inbred rat strains. Physiol Behav 1994, 369-373.
5. Armario A., Gabaldá A., Martí J. Comparison of the behavioural and endocrine response to forced swimming stress in five inbred strains of rats. Psychoneuroendocrinology 1994, 20:879-890.
6. Athey G.R., Iams S.G. Cold-restraint induced gastric lesions in normotensive and spontaneously hypertensive rats. Life Sci 1981, 28:889-894.
7. Boix F., Fernández-Teruel A., Tobeña A. The anxiolytic action of benzodiazepines is not present in handling-habituated rats. Pharmacol Biochem Behav 1988, 31:541-546.
8. Braw Y., Malkesman O., Dagan M., Bercovich A., Lavi-Avnon Y., Schroeder M., et al. Anxiety-like behaviours in pre-pubertal rats of the flinders sensitive lines (FSL) and Wistar-Kyoto (WKY) animal models of depression. Behav Brain Res 2006, 167:261-269.
9. Carrasco J., Márquez C., Nadal R., Tobeña A., Fernández-Teruel A., Armario A. Characterization of central and peripheral components of the hypothalamus-pituitary-adrenal axis in the inbred Roman rat strains. Psychoneuroendocrinology 2008, 33:437-445.
10. Castanon N., Dulluc J., Le Moal M., Mormêde P. Prolactin as a link between behavioral and immune differences between the Roman rat lines. Physiol Behav 1992, 51:1235-1241.
11. Castanon N., Pérez-Díaz F., Mormede P. Genetic analysis of the relationship between behavioral and neuroendocrine traits in Roman high and low avoidance rat lines. Behav Genet 1995, 25:371-383.
12. Craft R.M., Kostick M.L., Rogers J.A., White C.L., Tsutsui K.T. Forced swim test behavior in postpartum rats. Pharmacol Biochem Behav 2010, 96:402-412.
13. Detke M., Rickels M., Lucki I. Active behaviors in the rat forced swimming test differentially activated by serotonergic and noradrenergic antidepressants. Psychopharmacology (Berl) 1995, 121:66-72.
14. Driscoll P., Escorihuela R.M., Fernández-Teruel A., Giorgi O., Schwegler H., Steimer T.H., et al. Genetic selection and differential stress responses. Ann NY Acad Sci 1998, 851:501-510.
15. Driscoll P., Fernández-Teruel A., Corda M.G., Giorgi O., Steimer T. Some guidelines for defining personality differences in rats. Handbook of behavior genetics 2009, 281-300. Springer, New York. K. Yong-Kyu (Ed.).
16. Escorihuela R.M., Fernández-Teruel A., Gil L., Aguilar R., Tobeña A., Driscoll P. Inbred Roman high- and low- avoidance rats: differences in anxiety, novelty-seeking, and shuttlebox behaviors. Physiol Behav 1999, 67:19-26.
17. Escorihuela R.M., Fernández-Teruel A., Zapata A., Núñez J.F., Tobeña A. Flumazenil prevents the anxiolytic effects diazepam, alprazolam and adinazolam on the early acquisition of two-way active avoidance. Pharmacol Res 1993, 28:53-58.
18. Escorihuela R.M., Tobeña A., Driscoll P., Fernández-Teruel A. Effects of training, early handling, and perinatal flumazenil on shuttle box acquisition in Roman low-avoidance rats: toward overcoming a genetic deficit. Neurosci Biobehav Rev 1995, 19:353-367.
19. Fernández-Teruel A., Escorihuela R.M., Boix F., Tobeña A. Effects of different handling-stimulation procedures and benzodiazepines on two-way active avoidance acquisition in rats. Pharmacol Res 1991, 24:273-282.
20. Fernández-Teruel A., Escorihuela R.M., Gray J.A., Aguilar R., Gil L., Giménez-Llort L., et al. A quantitative trait locus influencing anxiety in the laboratory rat. Genome Res 2002, 12:618-626.
21. Fernández-Teruel A., Escorihuela R.M., Núñez J.F., Zapata A., Boix F., Salazar W., et al. The early acquisition of two-way (shuttle-box) avoidance as an anxiety-mediated behavior: psychopharmacological validation. Brain Res Bull 1991, 26:173-176.
22. Fernández-Teruel A., Escorihuela R.M., Tobeña A., Driscoll P. Stress and putative endogenous ligands for benzodiazepine receptors: the importance of characteristics of the aversive situation and of differential emotionality in experimental animals. Experientia 1991, 47:1051-1056.
23. Freeman M.E., Kanyicska B., Lerant A., Nagy G. Prolactin: structure, function and regulation of secretion. Physiol Rev 2001, 80:1523-1631.
24. Gomez F., Lahmame A., de Kloet E.R., Armario A. Hypothalamic-pituitary-adrenal response to chronic stress in five inbred rat strains: differential responses are mainly located at the adrenocortical level. Neuroendocrinology 1996, 63:327-337.
25. Hansen C., Spuhler K. Development of the National Institutes of Health genetically heterogeneous stock. Alcohol Clin Exp Res 1984, 8:477.
26. Johannesson M., López-Aumatell R., Stridh P., Diez M., Tuncel J., Blázquez G., et al. A resource for the simultaneous high-resolution mapping of multiple quantitative trait loci in rats: the NIH heterogeneous stock. Genome Res 2008, 19:150-158.
27. Koolhaas J.M., Bartolomucci A., Buwalda B., de Boer S.F., Flügge G., Korte S.M., et al. Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev 2011, 35:1291-2130.
28. Korte S.M., Koolhaas J.M., Wingfi{ligature}eld J.C., McEwen B.S. The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neurosci Biobehav Rev 2005, 29:3-38.
29. Lahmame A., Grigoriadis D.E., De Souza E.B., Armario A. Brain corticotropin-releasing factor immunoreactivity and receptors in five inbred rat strains: relationship to forced swimming behaviour. Brain Res 1997, 750:285-292.
30. Ledoux J.E., Sakaguchi A., Reis D.J. Strain differences in fear between spontaneously hypertensive and normotensive rats. Brain Res 1983, 277:137-143.
31. López-Aumatell R., Blázquez G., Gil L., Aguilar R., Cañete T., Giménez-Llort L., et al. The Roman high- and low-avoidance rat strains differ in fear-potentiated startle and classical aversive conditioning. Psicothema 2009, 21:27-32.
32. López-Aumatell R., Guitart-Masip M., Vicens-Costa E., Giménez-Llort L., Valdar W., Johannesson M., et al. Fearfulness in a large N/Nih genetically heterogeneous rat stock: differential profiles of timidity and defensive flight in males and females. Behav Brain Res 2008, 188:41-55.
33. López-Aumatell R., Vicens-Costa E., Guitart-Masip M., Martínez-Membrives M., Valdar W., Johannesson M., et al. Unlearned anxiety predicts learned fear: a comparison among heterogeneous rats and the Roman rat strains. Behav Brain Res 2009, 202:92-101.
34. Malkesman O., Braw Y., Maayan R., Weizman A., Overstreet D.H., Shabat-Simon M., et al. Two different putative genetic animal models of childhood depression. Biol Psychiatry 2006, 59:17-23.
35. Malkesman O., Braw Y., Zagoory-Sharon O., Golan O., Lavi-Avnon Y., Schroeder M., et al. Reward and anxiety in genetic animal models of childhood depression. Behav Brain Res 2005, 164:1-10.
36. Núñez J.F., Ferré P., Escorihuela R.M., Tobeña A., Fernández-Teruel A. Effects of handling of rats on emotional, HPA-Axis, and prolactin reactivity to novelty and conflicto. Physiol Behav 1996, 60:1355-1359.
37. Núñez J.F., Ferré P., García E., Escorihuela R.M., Fernández-Teruel A., Tobeña A. Postnatal handling reduces emotionality ratings and accelerates two-way active avoidance in female rats. Pharmacol Biochem Behav 1995, 51:199-203.
38. Onaka T., Takayanagi Y., Leng G. Metabolic and stress-related roles of prolactin-releasing peptide. Trends Endocrinol Metab 2010, 21:287-293.
39. Pähkla R., Kask A., Rägo L. Differential effects of beta-carbolines and antidepressants on rat exploratory activity in the elevated zero-maze. Pharmacol Biochem Behav 2000, 65:737-742.
40. Paré W.P. Behavioral despair test predicts stress ulcer in WKY rats. Physiol Behav 1989, 46:483-487.
41. Paré W.P. Stress ulcer susceptibility and depression in wistar Kyoto (WKY) rats. Physiol Behav 1989, 46:993-998.
42. Paré W.P. The performance of WKY rats on three tests of emotional behaviour. Physiol Behav 1992, 51:1051-1056.
43. Paré W.P. Open field, learned helplessness, conditioned defensive burying, and forced swim test in WKY rats. Physiol Behav 1994, 55:433-439.
44. Paré W.P., Redei E. Depressive behaviour and stress ulcer in Wistar-Kyoto rats. J Physiol (Paris) 1993, 87:229-238.
45. Paré W.P. Open-field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats. Pshysiol Behav 1994, 55:433-439.
46. Piras G., Barbato A., Giorgi O., Corda M. Effects of antidepressants on the performance in the forced swim test of two psychogenetically selected lines of rats that differ in coping strategies to aversive condictions. Psychopharmacology (Berl) 2010, 211:403-414.
47. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model to antidepressant treatments. Nature 1977, 266:730-732.
48. Prunell M., Escorihuela R.M., Fernández-Teruel A., Núñez J.F., Tobeña A. Differential interactions between ethanol and Ro 15-4513 on two anxiety tests in rats. Pharmacol Biochem Behav 1994, 47:147-151.
49. Prunell M., Escorihuela R.M., Fernández-Teruel A., Núñez J.F., Tobeña A. Anxiolytic profiles of alprazolam and ethanol in the elevated plus-maze test and the early acquisition of shuttle-box avoidance. Pharmacol Res 1994, 29:37-45.
50. Ratner A., Yelvington D.B., Rosenthal M. Prolactin and corticosterone response to repeated footshock stress in male rats. Psychoneuroendocrinology 1989, 14:393-396.
51. Redei E., Pare W.P., Aird F., Klucynski J. Strain differences in hypothalamic-pituitary-adrenal activity and stress ulcer. Am J Physiol 1994, 266:R353-R360.
52. Ribeiro M.F., Ferigolo M., Reis F.M., Barros H.M., Spritzer P.M. Paradoxical effect of imipramine in hyperprolactinemic female rats exposed to the forced swimming test. Physiol Behav 2000, 68:619-623.
53. Sabariego M., Gómez M.J., Morón I., Torres C., Fernández-Teruel A., Tobeña A., Cañete T., Martínez-Conejero J.A., Horcajadas J.A., Esteban F.J. Differential gene expression between inbred Roman high- (RHA-I) and low- (RLA-I) avoidance rats. Neurosci lett 2011, 504:265-270.
54. Servatius R.J., Ottenweller J.E., Beldowizc D., Guo W., Zhu G., Natelson B.H. Persistenly exaggerated startle responses in rats treated with pyridostigmine bromide. J Pharmacol Exp Ther 1998, 287:1020-1028.
55. Shepherd J.K., Grewal S.S., Fletcher A., Bill D.J., Dourish C.T. Behavioural and pharmacological characterisation of the elevated zero-maze as an animal model of anxiety. Psychopharmacology (Berl) 1994, 116:56-64.
56. Solberg L.C., Holl K., Tschannen M., Valdar W. Fine-mapping a locus for glucose tolerance using heterogeneous stock rats. Physiol Genomics 2010, 41:102-108.
57. Solberg L.C., Olson S.L., Turek F.W., Redei E. Altered hormone levels and circadian rhythm of activity in the WKY rat, a putative animal model of depression. Am J Physiol-Reg I 2001, 281:R786-R794.
58. Spuhler K., Dietrich R.A. Correlative analysis of ethanol-related phenotypes in rat inbred strains. Alcohol Clin Exp Res 1984, 8:480-484.
59. Steimer T., Driscoll P. Divergent stress responses and coping styles in psychogenetically selected Roman high-(RHA) and low-(RLA) avoidance rats: behavioral, neuroendocrine and developmental aspects. Stress 2003, 6:87-100.
60. Steimer T., Driscoll P. Inter-individual vs line/strain differences in psychogenetically selected Roman High-(RHA) and Low-(RLA) avoidance rats: neuroendocrine and behavioural aspects. Neurosci Biobehav Rev 2005, 29:99-112.
61. Steimer T., Escorihuela R.M., Fernández-Teruel A., Driscoll A. Long-term behavioural and neuroendocrine changes in Roman High- (RHA/Verh) and Low-(RLA/verh) Avoidance rats following neonatal handling. Int J Dev Neurosci 1998, 5:54-63.
62. Steimer T., la Fleur S., Schulz P.E. Neuroendocrine correlates of emotional reactivity and coping in male rats from the Roman High (RHA/Verh)- and Low (RLA/Verh)-Avoidance lines. Behav Genet 1997, 27:503-512.
63. Telner J.I., Merali Z., Singhal R.L. Stress controllability and plasma prolactin levels in the rat. Psychoneuroendocrinology 1982, 7:361-364.
64. Vicens-Costa E., Martínez-Membrives E., López-Aumatell R., Guitart-Masip M., Cañete T., Blázquez G., et al. Two-way avoidance acquisition is negatively related to conditioned freezing and positively associated with startle reactions: a dissection of anxiety and fear in genetically heterogeneous rats. Physiol Behav 2011, 103:148-156.
65. Yelvington D.B., Weiss G.K., Ratner A. Effect of corticosterone on the prolactin response to psychological and physical stress in rats. Life Sci 1984, 35:1705-1711.
66. Yelvington D.B., Weiss G.K., Ratner A. Habituation of the prolactin response in rats to psychological stress. Psychoneuroendocrinology 1985, 10:95-102.