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

Author
item RAULT, JEAN-LOUP - Purdue University
item MACK, LAURIE - Purdue University
item CARTER, C. SUE - University Of Illinois
item GARNER, JOSEPH - Purdue University
item Marchant, Jeremy
item RICHERT, BRIAN - Purdue University
item Lay Jr, Donald

Submitted to: Applied Animal Behaviour Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/1/2013
Publication Date: 9/1/2013
Citation: Rault, J., Mack, L.A., Carter, C., Garner, J.P., Marchant Forde, J.N., Richert, B.T., Lay Jr., D.C. 2013. Prenatal stress puzzle, the oxytocin piece: Prenatal stress alters the behaviour and autonomic regulation in piglets, insights from oxytocin. Applied Animal Behaviour Science. 148(1-2):99-107.

Interpretive Summary: Developmental changes in response to prenatal stressors have been proposed to constitute an adaptive strategy aimed to enhance offspring’s survival traits. Prenatal stressors of diverse natures, whether it be nutritional, physical, or physiological can have long-lasting physiological and behavioral consequences. However, the same strategies that have evolved as adaptive in natural environments may be maladaptive in captive environments. Captive animals are usually kept at high densities relative to their wild counterparts. Unnatural social group dynamics, such as maintaining animals at high densities, in uniform sex and age groups, or mixing them with unfamiliar peers can all contribute to social stress, while disturbing the use of evolutive social strategies such as hierarchy or social support. Spatial and social constraints are intrinsic to animal holding facilities, and could affect both the dams and their offspring. The welfare implications of prenatal stress on the offspring are highly relevant to animals kept in captive environments. Prenatal stress can alter the offspring’s behavior, leading to anxiety-related behaviors, cognitive deficits, and abnormal social development. Oxytocin is a mammalian neuropeptide with a major involvement in various social processes. In particular, elevated oxytocin reduces anxiety in rodents whereas oxytocin deficiency results in impaired social behavior. Therefore, oxytocin appears to bestow effects opposite to the anxiety and social deficits seen in prenatally stressed offspring. Thus to determine if oxytocin could reverse the effects of prenatal stress; female offspring from 3 socially stressed (35-56 days of gestation) and 3 control sows were tested. In each litter, 2 piglets received oxytocin intranasally and 2 piglets saline. After 45 min, each piglet was isolated for 15 minutes to determine its response to stress. Prenatally stressed piglets from socially stressed sows displayed lower levels of behavioral arousal and heart rate during social isolation. The administration of oxytocin to prenatally stressed piglets reestablished vigilance behaviors such as alertness and standing. Both control and prenatally stressed piglets had lower heart rate following oxytocin administration. These results suggest that social stress during the second trimester of gestation alters the development of the autonomic nervous system in the sow’s offspring. In conclusion, prenatal stress from a social origin resulted in female offspring displaying a lower behavioral and physiological arousal to social isolation. These behavioral modifications induced by prenatal stress can be reversed to some extent by oxytocin administration, suggesting a common physiological basis. These findings suggest that social stress in the second trimester of gestation alters the development of the autonomic nervous system in the pig’s offspring, which oxytocin administration helped to highlight.

Technical Abstract: Developmental changes in response to prenatal stressors (PNS) may represent an adaptive strategy to enhance survival traits in the offspring. Yet, PNS could be maladaptive for captive animals, causing anxiety and abnormal social development. Oxytocin (OT) reduces anxiety, whereas OT deficiencies are associated with social behavior deficits. Oxytocin could reverse PNS effects. Female offspring from 3 socially stressed (PNS 35-56 days of gestation) and 3 control sows were tested. In each litter, 2 piglets received 24 IU of OT intranasally and 2 piglets saline. After 45 min, each piglet was isolated for 15 min. PNS piglets performed less (PL.01)locomotion, escape attempts, alert behavior, and had a lower (PL.01)heart rate than control piglets. Oxytocin administration reestablished their alert and standing behaviors. Oxytocin resulted in a lower heart rate for all piglets and enhanced the parasympathetic tone of control, but not PNS, piglets. Social stress in mid-gestation alters the autonomic regulation and behavior of the offspring, discussed here in the context of the evolution of the mammalian autonomic nervous system.