Cortisol administration to pregnant sows affects novelty-induced locomotion, aggressive behaviour, and blunts gender differences in their offspring

Hormones and Behavior

Volumn 49, Issue 5, 2006, Pages 663-672

  Kranendonk, Godelieve ^a   Hopster, Hans ^b   Fillerup, Maaike ^b   Ekkel, E Dinand ^b   Mulder, Eduard J H ^c   Taverne, Marcel A M ^a  

^a Faculty of Veterinary Medicine   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Activity; Aggression; Behavioural tests; Corticosteroids; Gender differences; Gestation; Pig; Prenatal stress

Indexed keywords

CORTICOSTEROID; HYDROCORTISONE; HYDROCORTISONE ACETATE;

AGGRESSION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTIFICIAL INSEMINATION; BEHAVIOR; CONTROLLED STUDY; FEMALE; FIGHTING; GESTATION PERIOD; LOCOMOTION; MALE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROGENY; SALIVA LEVEL; SEX DIFFERENCE; SOCIALIZATION; STRESS; SWINE; VOCALIZATION; WALKING; WEANING;

AGGRESSION; ANIMALS; ANTI-INFLAMMATORY AGENTS; EXPLORATORY BEHAVIOR; FEMALE; HYDROCORTISONE; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SALIVA; SEX CHARACTERISTICS; SUS SCROFA;

EID: 33646141624     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2005.12.008     Document Type: Article

References (70)

1. Barbazanges A., Piazza P.V., Le Moal M., and Maccari S. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J. Neurosci. 16 12 (1996) 3943-3949
2. Bolhuis J.E., Schouten W.G.P., Leeuw J.A.D., Schrama J.W., and Wiegant V.M. Individual coping characteristics, rearing conditions and behavioural flexibility in pigs. Behav. Brain Res. 152 2 (2004) 351-360
3. Bolhuis J.E., Schouten W.G.P., Schrama J.W., and Wiegant V.M. Individual coping characteristics, aggressiveness and fighting strategies in pigs. Anim. Behav. 69 5 (2005) 1085-1091
4. Bowman R.E., MacLusky N.J., Sarmiento Y., Frankfurt M., Gordon M., and Luine V.N. Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology 145 8 (2004) 3778-3787
5. Braastad B.O., Osadchuk L.V., Lund G., and Bakken M. Effects of prenatal handling stress on adrenal weight and function and behaviour in novel situations in blue fox cubs (Alopex lagopus). Appl. Anim. Behav. Sci. 57 1-2 (1998) 157-169
6. Clarke A.S., Wittwer D.J., Abbott D.H., and Schneider M.L. Long-term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys. Dev. Psychobiol. 27 5 (1994) 257-269
7. Clarke A.S., Soto A., Bergholz T., and Schneider M.L. Maternal gestational stress alters adaptive and social behavior in adolescent rhesus monkey offspring. Infant Behav. Dev. 19 (1996) 451-461
8. D'Eath R.B. Individual aggressiveness measured in a resident-intruder test predicts the persistence of aggressive behaviour and weight gain of young pigs after mixing. Appl. Anim. Behav. Sci. 77 4 (2002) 267-283
9. Deminière J.M., Piazza P.V., Guegan G., Abrous N., Maccari S., Le Moal M., and Simon H. Increased locomotor response to novelty and propensity to intravenous amphetamine self-administration in adult offspring of stressed mothers. Brain Res. 586 1 (1992) 135-139
10. Diaz R., Fuxe K., and Ogren S.O. Prenatal corticosterone treatment induces long-term changes in spontaneous and apomorphine-mediated motor activity in male and female rats. Neuroscience 81 1 (1997) 129-140
11. Donaldson T.M., Newberry R.C., Spinka M., and Cloutier S. Effects of early play experience on play behaviour of piglets after weaning. Appl. Anim. Behav. Sci. 79 3 (2002) 221-231
12. Engel B., and Keen A. A simple approach for the analysis of generalized linear mixed models. Stat. Neerl. 48 (1994) 1-22
13. Erhard H.W., and Mendl M. Measuring aggressiveness in growing pigs in a resident-intruder situation. Appl. Anim. Behav. Sci. 54 2-3 (1997) 123-136
14. Faustini M., Munari E., Russo V., Pastorelli G., Restelli G.L., Scocca S., and Vigo D. Pig reactivity to backtest and growth during the first three months of life. Vet. Res. Commun. 28 (2004) 181-183
15. Fride E., and Weinstock M. The effects of prenatal exposure to predictable or unpredictable stress on early development in the rat. Dev. Psychobiol. 17 6 (1984) 651-660
16. Fride E., Dan Y., Feldon J., Halevy G., and Weinstock M. Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol. Behav. 37 5 (1986) 681-687
17. Giroux S., Martineau G.P., and Robert S. Relationships between individual behavioural traits and post-weaning growth in segregated early-weaned piglets. Appl. Anim. Behav. Sci. 70 (2000) 41-48
18. Haussmann M.F., Carroll J.A., Weesner G.D., Daniels M.J., Matteri R.L., and Lay D.C. Administration of ACTH to restrained, pregnant sows alters their pigs' hypothalamic-pituitary-adrenal (HPA) axis. J. Anim. Sci. 78 9 (2000) 2399-2411
19. Hemsworth P.H., Price E.O., and Borgwardt R. Behavioural responses of domestic pigs and cattle to humans and novel stimuli. Appl. Anim. Behav. Sci. 50 (1996) 43-56
20. Hessing M.J.C., Hagelso A.M., Beek J.A.M.v., Wiepkema P.R., Schouten W.G.P., and Krukow R. Individual behavioural characteristics in pigs. Appl. Anim. Behav. Sci. 37 (1993) 285-295
21. Huizink A.C., Mulder E.J., and Buitelaar J.K. Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility?. Psychol. Bull. 130 1 (2004) 115-142
22. Janczak A.M., Pedersen L.J., Rydhmer L., and Bakken M. Relation between early fear- and anxiety-related behaviour and maternal ability in sows. Appl. Anim. Behav. Sci 82 2 (2003) 121-135
23. Jarvis S., Moinard C., Robson S.K., Baxter E., Ormandy E., Douglas A.J., Seckl J.R., Russell J.A., and Lawrence A.B. Programming the offspring of the pig by prenatal social stress: neuroendocrine activity and behaviour. Horm. Behav. 49 1 (2006) 68-80
24. Jensen P., and Algers B. An ethogram of piglet vocalizations during suckling. Appl. Anim. Ethol. 11 3 (1984) 237-248
25. Jones J.B., Wathes C.M., White R.P., and Jones R.B. Do piglets find a familiar odourant attractive in novel surroundings?. Appl. Anim. Behav. Sci. 70 (2000) 115-126
26. Kaiser S., and Sachser N. Social stress during pregnancy and lactation affects in guinea pigs the male offsprings' endocrine status and infantilizes their behaviour. Psychoneuroendocrinology 26 5 (2001) 503-519
27. Kaiser S., Heemann K., Straub R.H., and Sachser N. The social environment affects behaviour and androgens, but not cortisol in pregnant female guinea pigs. Psychoneuroendocrinology 28 1 (2003) 67-83
28. Kaiser S., Kruijver F.P.M., Swaab D.F., and Sachser N. Early social stress in female guinea pigs induces a masculinization of adult behavior and corresponding changes in brain and neuroendocrine function. Behav. Brain Res. 144 1-2 (2003) 199-210
29. Kanitz E., Otten W., Tuchscherer M., and Manteuffel G. Effects of prenatal stress on corticosteroid receptors and monoamine concentrations in limbic areas of suckling piglets (Sus scrofa) at different ages. J. Vet. Med., Ser. A 50 3 (2003) 132-139
30. Kanitz E., Tuchscherer M., Puppe B., Tuchscherer A., and Stabenow B. Consequences of repeated early isolation in domestic piglets (Sus scrofa) on their behavioural, neuroendocrine, and immunological responses. Brain Behav. Imm. 18 1 (2004) 35-45
31. Klemcke H.G., Sampath Kumar R., Yang K., Vallet J.L., and Christenson R.K. 11beta-hydroxysteroid dehydrogenase and glucocorticoid receptor messenger RNA expression in porcine placentae: effects of stage of gestation, breed, and uterine environment. Biol. Reprod. 69 6 (2003) 1945-1950
32. Koenig J.I., Elmer G.I., Shepard P.D., Lee P.R., Mayo C., Joy B., Hercher E., and Brady D.L. Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia. Behav. Brain Res. 156 2 (2005) 251-261
33. Korte S.M. Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci. Biobehav. Rev. 25 2 (2001) 117-142
34. Kranendonk G., Hopster H., Van Eerdenburg F.J.C.M., Van Reenen C.G., Fillerup M., De Groot J., Korte S.M., and Taverne M.A.M. Evaluation of oral administration of cortisol as a model for prenatal stress in pregnant sows. Am. J. Vet. Res. 66 5 (2005) 780-790
35. Kranendonk, G., Hopster, H., Fillerup, M., Ekkel, E.D., Mulder, E.J.H., Wiegant, V.M., Taverne, M.A.M., in press. Lower birth weight and attenuated adrenocortical response to ACTH in offspring from sows that orally received cortisol during gestation, Dom. Anim. Endocrinol.
36. Maccari S., Piazza P.V., Kabbaj M., Barbazanges A., Simon H., and Le Moal M. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J. Neuroci. 15 1 (1995) 110-116
37. Marchlewska-Koj A., Kapusta J., and Kruczek M. Prenatal stress modifies behavior in offspring of bank voles (Clethrionomys glareolus). Physiol. Behav. 79 4-5 (2003) 671-678
38. Martin P., and Bateson P. Measuring Behaviour (1993), Cambridge Univ. Press, Cambridge, UK
39. Matthews S.G. Antenatal glucocorticoids and programming of the developing CNS. Ped. Res. 47 3 (2000) 291-300
40. Meese G.B., and Ewbank R. The establishment and nature of the dominance hierarchy in the domesticated pig. Anim. Behav. 21 (1973) 326-334
41. Moriceau S., and Sullivan R.M. Corticosterone influences on Mammalian neonatal sensitive-period learning. Behav. Neurosci. 118 2 (2004) 274-281
42. Newberry R.C., Špinka M., and Cloutier S. Early social experience of piglets affects rate of adaptation to strangers after weaning. Proceedings of the 34th International Congress of the ISAE, Florianópolis, Brazil, 17-20 October (2000) 67
43. Nishio H., Kasuga S., Ushijima M., and Harada Y. Prenatal stress and postnatal development of neonatal rats-Sex- dependent effects on emotional behavior and learning ability of neonatal rats. Int. J. Dev. Neurosci. 19 1 (2001) 37-45
44. Owen D., Andrews M.H., and Matthews S.G. Maternal adversity, glucocorticoids and programming of neuroendocrine function and behaviour. Neurosci. Biobehav. Rev. 29 2 (2005) 209-226
45. Payne R.W. The Guide to GenStat® Release 7.1. VSN International (2003) Oxford, UK
46. Pepe G.J., and Albrecht E.D. Comparison of cortisol-cortisone interconversion in vitro by the human and baboon placenta. Steroids 44 3 (1984) 229-240
47. Roussel S., Hemsworth P.H., Boissy A., and Duvaux-Ponter C. Effects of repeated stress during pregnancy in ewes on the behavioural and physiological responses to stressful events and birth weight of their offspring. Appl. Anim. Behav. Sci. 85 3-4 (2004) 259-276
48. Roussel S., Boissy A., Montigny D., Hemsworth P.H., and Duvaux-Ponter C. Gender-specific effects of prenatal stress on emotional reactivity and stress physiology of goat kids. Horm. Behav. 47 3 (2005) 256-266
49. Ruis M.A.W., Brake J.H.A.t., Engel B., Ekkel E.D., Buist W.G., Blokhuis H.J., and Koolhaas J.M. The circadian rhythm of salivary cortisol in growing pigs: effects of age, gender, and stress. Physiol. Behav. 62 3 (1997) 623-630
50. Ruis M.A.W., te B.J.H.A., Burgwal J.A.v.d., Jong I.C.d., Blokhuis H.J., and Koolhaas J.M. Personalities in female domesticated pigs: behavioural and physiological indications. Appl. Anim. Behav. Sci. 66 1-2 (2000) 31-47
51. Schneider M.L. Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus monkey infants. Dev. Psychobiol. 25 7 (1992) 529-540
52. Schneider M.L., Roughton E.C., Koehler A.J., and Lubach G.R. Growth and development following prenatal stress exposure in primates: an examination of ontogenetic vulnerability. Child Dev. 70 2 (1999) 263-274
53. Schouten, W.G.P., 1986. Rearing conditions and behavior in pigs. PhD thesis, Wageningen Agricultural University, The Netherlands.
54. Seckl J.R. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol. Cell. Endocrinol. 185 1-2 (2001) 61-71
55. Suchecki D., and Palermo Neto J. Prenatal stress and emotional response of adult offspring. Physiol. Behav. 49 3 (1991) 423-426
56. Takahashi L.K., Haglin C., and Kalin N.H. Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats. Physiol. Behav. 51 2 (1992) 319-323
57. Takahashi L.K., Turner J.G., and Kalin N.H. Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats. Brain Res. 574 1-2 (1992) 131-137
58. Tazumi T., Hori E., Uwano T., Umeno K., Tanebe K., Tabuchi E., Ono T., and Nishijo H. Effects of prenatal maternal stress by repeated cold environment on behavioral and emotional development in the rat offspring. Behav. Brain Res. 162 1 (2005) 153-160
59. Vallée M., Mayo W., Dellu F., Le Moal M., Simon H., and Maccari S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J. Neurosci. 17 7 (1997) 2626-2636
60. Van den Bergh B.R., and Marcoen A. High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Dev. 75 4 (2004) 1085-1097
61. Van Erp-Van der Kooij E., Kuijpers A.H., Schrama J.W., Ekkel E.D., and Tielen M.J.M. Individual behavioural characteristics in pigs and their impact on production. Appl. Anim. Behav. Sci. 66 (2000) 171-185
62. Van Erp-Van der Kooij E., Kuijpers A.H., Van Eerdenburg F.J.C.M., and Tielen M.J.M. A note on the influence of starting position, time of testing and test order on the backtest in pigs. Appl. Anim. Behav. Sci. 73 4 (2001) 263-266
63. Van Erp-Van der Kooij E., Kuijpers A.H., Schrama J.W., van Eerdenburg F.J.C.M., Schouten W.G.P., and Tielen M.J.M. Can we predict behaviour in pigs? Searching for consistency in behaviour over time and across situations. Appl. Anim. Behav. Sci. 75 4 (2002) 293-305
64. Van Putten G., and Buré R.G. Preparing gilts for group housing by increasing their social skills. Appl. Anim. Behav. Sci. 54 (1997) 173-183
65. Waddell B.J., Hisheh S., Dharmarajan A.M., and Burton P.J. Apoptosis in rat placenta is zone-dependent and stimulated by glucocorticoids. Biol. Reprod. 63 (2000) 1913-1917
66. Weinstock M. Does prenatal stress impair coping and regulation of hypothalamic- pituitary-adrenal axis?. Neurosci. Biobehav. Rev. 21 1 (1997) 1-10
67. Weinstock M. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog. Neurobiol. 65 5 (2001) 427-451
68. Welberg L.A., Seckl J.R., and Holmes M.C. Inhibition of 11beta-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring. Eur. J. Neurosci. 12 3 (2000) 1047-1054
69. Wemelsfelder F., Haskell M., Mendl M.T., Calvert S., and Lawrence A.B. Diversity of behaviour during novel object tests is reduced in pigs housed in substrate-impoverished conditions. Anim. Behav. 60 3 (2000) 385-394
70. Ziecik A.J., Esbenshade K.L., Howard H.J., and Britt J.H. Sex-related differences in the control of gonadotropin concentrations in neonatal pigs. Anim. Reprod. Sci. 23 2 (1990) 123-133