Prenatal stress puzzle, the oxytocin piece: Prenatal stress alters the behaviour and autonomic regulation in piglets, insights from oxytocin

Applied Animal Behaviour Science

Volumn 148, Issue 1-2, 2013, Pages 99-107

  Rault, Jean Loup ^a   Mack, Laurie A ^a   Carter, C Sue ^b   Garner, Joseph P ^a   Marchant, Jeremy N ^c   Richert, Brian T ^a   Lay, Donald C ^c  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

Behaviour; Heart rate; Offspring; Oxytocin; Prenatal stress; Social

Indexed keywords

AGE; BEHAVIORAL ECOLOGY; BEHAVIORAL RESPONSE; FEMALE; NERVOUS SYSTEM; PIG; PREGNANCY; SOCIAL BEHAVIOR; SOCIAL DEVELOPMENT;

EID: 84884354145     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.applanim.2013.07.001     Document Type: Article

References (71)

1. Aleksandrov A.A., Polyakova O.N., Batuev A.S. The effects of prenatal stress on learning in rats in a Morris maze. Neurosci. Behav. Physiol. 2001, 31:71-74.
2. Amico J. Conditional oxytocin receptor knockout mice: targeting the forebrain to understand behavior. Endocrinology 2008, 149:3254-3255.
3. Arey D.S. Time course for the formation and disruption of social organisation in group-housed sows. Appl. Anim. Behav. Sci. 1999, 62:199-207.
4. Barnett J.L., Hemsworth P.H., Cronin G.M., Newman E.A., McCallum T.H. Effects of design of individual cage-stalls on the behavioural and physiological responses related to the welfare of pregnant pigs. Appl. Anim. Behav. Sci. 1991, 32:23-33.
5. Batuev A.S., Polyakova O.N., Aleksandrov A.A. The effect of prenatal "social stress" on anxiety. Zhurnal Vysshei Nervnoi Deyatelnosti Imeni I P Pavlova 2000, 50:281-286.
6. Berntson G.G., Lozano D.L., Chen Y.-J. Filter properties of root mean square successive difference (RMSSD) for heart rate. Psychophysiology 2005, 42(2):246-252.
7. Blume A., Bosch O.J., Miklos S., Torner L., Wales L., Waldherr M., Neumann I.D. Oxytocin reduces anxiety via ERK1/2 activation: local effect within the rat hypothalamic paraventricular nucleus. Eur. J. Neurosci. 2008, 27:1947-1956.
8. Bos P.A., Panksepp J., Bluthé R.-M., Honk J.v. Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: a review of single administration studies. Front. Neuroendocrinol. 2012, 33:17-35.
9. Born J., Lange T., Kern W., McGregor G.P., Bickel U., Fehm H.L. Sniffing neuropeptides: a transnasal approach to the human brain. Nat. Neurosci. 2002, 5:514-516.
10. Braastad B.O. Effects of prenatal stress on behaviour of offspring of laboratory and farmed mammals. Appl. Anim. Behav. Sci. 1998, 61:159-180.
11. Brown A.S., van Os J., Driessens C., Hoek H.W., Susser E.S. Further evidence of relation between prenatal famine and major affective disorder. Am. J. Psychiatry 2000, 157:190-195.
12. Carter C.S. Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 1998, 23:779-818.
13. Carter C.S. Developmental consequences of oxytocin. Physiol. Behav. 2003, 79:383-397.
14. Carter C.S. Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders?. Behav. Brain Res. 2007, 176:170-186.
15. Clarke A.S., Schneider M.L. Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys. Dev. Psychobiol. 1993, 26:293-304.
16. Coulon M., Hild S., Schroeer A., Janczak A.M., Zanella A.J. Gentle vs. aversive handling of pregnant ewes: II. Physiology and behavior of the lambs. Physiol. Behav. 2011, 103:575-584.
17. Davis B. The effect of prenatal stress on the physiological and behavioral development of offspring 2010, 110. Animal Sciences, Texas Tech University, Lubbock, TX, USA, (M.S. Thesis).
18. Dreifuss J.J., Raggenbass M., Charpak S., Dubois-Dauphin M., Tribollet E. A role of central oxytocin in autonomic functions: its action in the motor nucleus of the vagus nerve. Brain Res. Bull. 1988, 20:765-770.
19. Emiliano A.B.F., Cruz T., Pannoni V., Fudge J.L. The interface of oxytocin-labeled cells and serotonin transporter-containing fibers in the primate hypothalamus: a substrate for SSRIs therapeutic effects?. Neuropsychopharmacology 2007, 32:977-988.
20. Engelmann M., Landgraf R., Wotjak C.T. The hypothalamic-neurohypophysial system regulates the hypothalamic-pituitary-adrenal axis under stress: an old concept revisited. Front. Neuroendocrinol. 2004, 25:132-149.
21. Estevez I., Andersen I.-L., Naævdal E. Group size, density and social dynamics in farm animals. Appl. Anim. Behav. Sci. 2007, 103:185-204.
22. FASS Guide for the Care and Use of Agricultural Animals in Research and Teaching 2010, Federation of Animal Science Societies, Champaign, IL, USA, Available at: http://www.fass.org/docs/agguide3rd/Ag_Guide_3rd_ed.pdf#page=16.
23. Fride E., Weinstock M. Prenatal stress increases anxiety related behavior and alters cerebral lateralization of dopamine activity. Life Sci. 1988, 42:1059-1065.
24. Gonyou H.W. The social behaviour of pigs. Social Behaviour in Farm Animals 2001, 147-168. CABI Publishing, Wallingford, UK. L.J. Keeling, H.W. Gonyou (Eds.).
25. Grippo A.J., Trahanas D.M., Zimmerman R.R., Porges S.W., Carter C.S. Oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation. Psychoneuroendocrinology 2009, 34:1542-1553.
26. Gutkowska J., Jankowski M., Lambert C., Mukaddam-Daher S., Zingg H., McCann S. Oxytocin releases atrial natriuretic peptide by combining with oxytocin receptors in the heart. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:11704-11709.
27. Haussmann M.F., Carroll J.A., Weesner G.D., Daniels M.J., Matteri R.L., Lay D.C. Administration of ACTH to restrained, pregnant sows alters their pigs hypothalamic-pituitary-adrenal (HPA) axis. J. Anim. Sci. 2000, 78:2399-2411.
28. Hay M., Meunier-Salaun M.C., Brulaud F., Monnier M., Mormede P. Assessment of hypothalamo-pituitary-adrenal axis and sympathetic nervous system activity in pregnant sows through the measurement of glucocorticoids and catechnolamines in urine. J. Anim. Sci. 2000, 78:420-428.
29. Heinrichs M., Baumgartner T., Kirschbaum C., Ehlert U. Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol. Psychiatry 2003, 54:1389-1398.
30. Higa K.T., Mori E., Viana F.F., Morris M., Michelini L.C. Baroreflex control of heart rate by oxytocin in the solitary-vagal complex. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 282:R537-R545.
31. Insel T.R. Is social attachment an addictive disorder?. Phys. Behav. 2003, 79:351-357.
32. Jarvis S., Moinard C., Robson S.K., Baxter E., Ormandy E., Douglas A.J., Seckl J.R., Russell J.A., Lawrence A.B. Programming the offspring of the pig by prenatal social stress: neuroendocrine activity and behaviour. Horm. Behav. 2006, 49:68-80.
33. Kofman O. The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci. Biobehav. Rev. 2002, 26:457-470.
34. Kosfeld M., Heinrichs M., Zak P.J., Fischbacher U., Fehr E. Oxytocin increases trust in humans. Nature 2005, 435:673-676.
35. Kovacs G.L., Sarnyai Z., Szabo G. Oxytocin and addiction: a review. Psychoneuroendocrinology 1998, 23:945-962.
36. Kranendonk G., Hopster H., Fillerup M., Ekkel E.D., Mulder E.J.H., Taveme M.A.M. Cortisol administration to pregnant sows affects novelty-induced locomotion, aggressive behaviour, and blunts gender differences in their offspring. Horm. Behav. 2006, 49:663-672.
37. Lay D.C., Kattesh H.G., Cunnick J.E., Daniels M.J., McMunn K.A., Toscano M.J., Roberts M.P. Prenatal stress effects on pig development and response to weaning. J. Anim. Sci. 2008, 86:1316-1324.
38. Lee P.R., Brady D.L., Shapiro R.A., Dorsa D.M., Koenig J.I. Prenatal stress generates deficits in rat social behavior: reversal by oxytocin. Brain Res. 2007, 1156:152-167.
39. Lehmann J., Stohr T., Feldon J. Long-term effects of prenatal stress experience and postnatal maternal separation on emotionality and attentional processes. Behav. Brain Res. 2000, 107:133-144.
40. Lemaire V., Koehl M., Le Moal M., Abrous D.N. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:11032-11037.
41. Lieberman M.W. Early developmental stress and later behavior. Science 1963, 141:824-825.
42. Light K.C., Grewen K.M., Amico J.A. More frequent partner hugs and higher oxytocin levels are linked to lower blood pressure and heart rate in premenopausal women. Biol. Psychol. 2005, 69:5-21.
43. MacDonald E., Dadds M.R., Brennan J.L., Williams K., Levy F., Cauchi A.J. A review of safety, side-effects and subjective reactions to intranasal oxytocin in human research. Psychoneuroendocrinology 2011, 36:1114-1126.
44. Mack L., Eicher S., Johnson A., Lay D., Richert B., Pajor A. The influence of gestational housing on the behavior, physiology and welfare of the sow and their piglets 2012, Department of Animal Sciences, Purdue University, West Lafayette, (Ph.D. Thesis).
45. Marchant-Forde R.M., Marlin D.J., Marchant-Forde J.N. Validation of a cardiac monitor for measuring heart rate variability in adult female pigs: accuracy, artefacts and editing. Physiol. Behav. 2004, 80:449-458.
46. Merlot E., Couret D., Otten W. Prenatal stress, fetal imprinting and immunity. Brain Behav. Immun. 2008, 22:42-51.
47. Meyer-Linderberg A., Domes G., Kirsch P., Heinrichs M. Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat. Rev. Neurosci. 2011, 12:524-538.
48. Neumann I.D. Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J. Neuroendocrinol. 2008, 20:858-865.
49. Olausson H., Uvnas-Moberg K., Sohlstrom A. Postnatal oxytocin alleviates adverse effects in adult rat offspring caused by maternal malnutrition. Am. J. Physiol. Endocrinol. Metab. 2003, 284:E475-E480.
50. Otten W., Kanitz E., Tuchscherer M., Puppe b., Nurnberg G. Repeated administrations of adenocorticotropic hormone during gestation in gilts: effects on growth, behaviour and immune responses of their piglets. Livestock Sci. 2007, 106:261-270.
51. Peters D.A.V. Effects of maternal stress during different gestational periods on the serotonergic system in adult-rat offspring. Pharmacol. Biochem. Behav. 1988, 31:839-843.
52. Peyronnet J., Dalmaz Y., Ehrström M., Mamet J., Roux J.-C., Pequignot J.-M., Thorén P., Lagercrantz H. Long-lasting adverse effects of prenatal hypoxia on developing autonomic nervous system and cardiovascular parameters in rats. Pflüg. Arch. Eur. J. Physiol. 2002, 443:858-865.
53. Ponirakis A., Susman E.J., Stifter C.A. Negative emotionality and cortisol during adolescent pregnancy and its effects on infant health and autonomic nervous system reactivity. Dev. Psychobiol. 1998, 33:163-174.
54. Rault J.-L. Friends with benefits: social support and its relevance for farm animal welfare. Appl. Anim. Behav. Sci. 2012, 136:1-14.
55. Rault J.-L. Oxytocin as an indicator of welfare related to the social environment: investigation and potential 2011, Department of Animal Sciences, Purdue University, West Lafayette, IN, USA, (Ph.D. Thesis).
56. Ross H.E., Young L.J. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front. Neuroendocrinol. 2009, 30:534-547.
57. Sachser N., Hennessy M.B., Kaiser S. Adaptive modulation of behavioural profiles by social stress during early phases of life and adolescence. Neurosci. Biobehav. Rev. 2011, 35:1518-1533.
58. Schneider M.L., Clarke A.S., Kraemer G.W., Roughton E.C., Lubach G.R., Rimm Kaufman S., Schmidt D., Ebert M. Prenatal stress alters brain biogenic amine levels in primates. Dev. Psychopathol. 1998, 10:427-440.
59. Sheriff M.J., Krebs C.J., Boonstra R. The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J. Anim. Ecol. 2009, 78:1249.
60. Sohlstrom A., Carlsson C., Uvnas-Moberg K. Effects of oxytocin treatment in early life on body weight and corticosterone in adult offspring from ad libitum-fed and food-restricted rats. Biol. Neonate 2000, 78:33-40.
61. Sontag L.W. The significance of fetal environmental differences. Am. J. Obstet. Gynecol. 1941, 42:996-1003.
62. Stolba A., Wood-Gush.D.G.M. The behaviour of pigs in a semi-natural environment. Anim. Prod. 1989, 48:419-425.
63. Taylor S.E., Gonzaga G.C., Klein L.C., Hu P., Greendale G.A., Seeman T.E. Relation of oxytocin to psychological stress responses and hypothalamic-pituitary-adrenocortical axis activity in older women. Psychosom. Med. 2006, 68:238-245.
64. Thompson W.R. Influence of prenatal maternal anxiety on emotionality in young rats. Science 1957, 125:698-699.
65. Vallee M., Mayo W., Dellu F., LeMoal M., Simon H., Maccari S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J. Neurosci. 1997, 17:2626-2636.
66. Veening J.G., de Jong T., Barendregt H.P. Oxytocin-messages via the cerebrospinal fluid: behavioral effects; a review. Physiol. Behav. 2010, 101:193-210.
67. von Borell E., Langbein J., Despres G., Hansen S., Leterrier C., Marchant-Forde J., et al. Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals - a review. Physiol. Behav. 2007, 92:293-316.
68. Weinstock M. Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis?. Neurosci. Biobehav. Rev. 1997, 21:1-10.
69. Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci. Biobehav. Rev. 2008, 32:1073-1086.
70. Welberg L.A.M., Seckl J.R. Prenatal stress, glucocorticoids and the programming of the brain. J. Neuroendocrinol. 2001, 13:113-128.
71. Windle R.J., Gamble L.E., Kershaw Y.M., Wood S.A., Lightman S.L., Ingram C.D. Gonadal steroid modulation of stress-induced hypothalamo-pituitary-adrenal activity and anxiety behavior: role of central oxytocin. Endocrinology 2006, 147:2423-2431.