Discrimination learning and judgment bias in low birth weight pigs.

Low birth weight (LBW) is a risk factor for cognitive and emotional impairments in humans. In pigs, LBW is a common occurrence, but its effects on cognition and emotion have received only limited scientific attention. To assess whether LBW pigs suffer from impaired cognitive and emotional development, we trained and tested 21 LBW and 21 normal birth weight (NBW) pigs in a judgment bias task. Judgment bias is a measure of emotional state which reflects the influence of emotion on an animal's interpretation of ambiguous stimuli. Pigs were trained to perform a specific behavioral response to two auditory stimuli, predicting either a positive or negative outcome. Once pigs successfully discriminated between these stimuli, they were presented with intermediate, ambiguous stimuli. The pigs' responses to ambiguous stimuli were scored as optimistic (performance of 'positive' response) or pessimistic (performance of 'negative' response). Optimistic or pessimistic interpretation of an ambiguous stimulus is indicative of a positive or negative emotional state, respectively. We found LBW pigs to require more discrimination training sessions than NBW pigs to reach criterion performance, suggesting that LBW causes a mild cognitive impairment in pigs. No effects of LBW on judgment bias were found, suggesting a similar emotional state for LBW and NBW pigs. This was supported by comparable salivary and hair cortisol concentrations for both groups. It is possible the enriched housing conditions and social grouping applied during our study influenced these results.

Effects of parity and litter size on cortisol measures in commercially housed sows and their offspring.

Breeding sows are regularly exposed to on-farm stressors throughout the duration of their production period. The impact of such stressors may differ for primi- and multiparous sows, as sows could learn to cope with stressors as they gain experience with them. If parity affects stress in sows, it may also impact their prenatal offspring through differential maternal stress. In addition to parity, litter size is another potential factor involved in stress of sows and piglets. Larger litters may be a source of discomfort for gestating sows, while it can result in intra-uterine growth restriction of piglets. In the current study, we aimed to assess whether parity and litter size affect cortisol measures in breeding sows and their offspring. To do this, we measured salivary cortisol concentrations of 16 primiparous and 16 multiparous sows at three time points: 1) while sows were group housed, 2) after sows were separated from the group prior to moving to the farrowing unit and 3) after handling procedures. In addition, hair cortisol concentration was determined for the sows during late gestation and for their low birth weight (n = 63) and normal birth weight (n = 43) offspring on day 3 after birth, to reflect in-utero cortisol exposure. It was expected that if sows adapt to on-farm stressors, the more experienced, multiparous sows would show decreased stress responses in comparison to primiparous sows. However, we found a comparable acute stress response of primi- and multiparous sows to separation from the group. Handling procedures did not influence sows' salivary cortisol concentrations. Sows' hair cortisol concentration was positively correlated with litter size. Future research is needed to assess whether this finding reflects increased stress in sows carrying larger litters. Parity or litter size did not have a direct effect on their offspring's hair cortisol concentration. Larger litters did have a higher occurrence of low birth weight piglets. For these piglets, females had higher neonatal hair cortisol concentrations than males. Overall, our results indicate that breeding sows do not adapt to all on-farm stressors. In addition, litter size may influence HPA axis activity in both sows and piglets.

Low Birth Weight Impairs Acquisition of Spatial Memory Task in Pigs.

In commercial pig farming, an increasing number of low birth weight (LBW) piglets are born, due to selection for large litter sizes. While LBW piglets have a higher risk of pre-weaning mortality, a considerable number of these piglets survive to slaughter age. In humans, LBW is a risk factor for long-term cognitive impairments. In pigs, studies examining the post-weaning effects of LBW on cognition have reported contradictory results. Therefore, the current study aimed to assess the effects of LBW on cognitive development in pigs using an improved study design, by (1) testing a larger sample size than previous studies, (2) assessing acute and chronic stress responses to account for a potential altered stress response in LBW pigs, and (3) testing both female and male pigs to account for potential confounding effects of sex. Learning and memory of 20 LBW pigs and 20 normal birth weight (NBW) pigs, both groups consisting of 10 females and 10 males, were compared using a spatial holeboard task. In this task, pigs had to learn and remember the locations of hidden food rewards. After a pig had successfully acquired the task, it was presented with two successive reversal phases during which it was presented with a new configuration of reward locations. The holeboard allows for simultaneous assessment of working and reference memory, as well as measures of motivation, exploration, and behavioral flexibility. Mixed model ANOVAs revealed a transiently impaired reference memory performance of LBW pigs, implying they had more difficulty learning their reward configuration in the holeboard. Also, LBW piglets showed increased pre-weaning hair cortisol concentrations compared to their NBW siblings. No other effects of LBW were found. Sex had no direct or interaction effects on any measures of holeboard performance or stress. It is possible that the enriched housing conditions applied during our study had an ameliorating effect on our pigs' cognitive development. Overall, our results suggest LBW has a negative effect on post-weaning cognitive performance in pigs. This could have welfare consequences as cognitive skills are required for pigs to learn how to correctly respond to their environment.

Judgement bias in pigs is independent of performance in a spatial holeboard task and conditional discrimination learning.

Biases in judgement of ambiguous stimuli, as measured in a judgement bias task, have been proposed as a measure of the valence of affective states in animals. We recently suggested a list of criteria for behavioural tests of emotion, one of them stating that responses on the task used to assess emotionality should not be confounded by, among others, differences in learning capacity, i.e. must not simply reflect the cognitive capacity of an animal. We performed three independent studies in which pigs acquired a spatial holeboard task, a free choice maze which simultaneously assesses working memory and reference memory. Next, pigs learned a conditional discrimination between auditory stimuli predicting a large or small reward, a prerequisite for assessment of judgement bias. Once pigs had acquired the conditional discrimination task, optimistic responses to previously unheard ambiguous stimuli were measured in the judgement bias task as choices indicating expectation of the large reward. We found that optimism in the judgement bias task was independent of all three measures of learning and memory indicating that the performance is not dependent on the pig's cognitive abilities. These results support the use of biases in judgement as proxy indicators of emotional valence in animals.

Making Decisions under Ambiguity: Judgment Bias Tasks for Assessing Emotional State in Animals.

Judgment bias tasks (JBTs) are considered as a family of promising tools in the assessment of emotional states of animals. JBTs provide a cognitive measure of optimism and/or pessimism by recording behavioral responses to ambiguous stimuli. For instance, a negative emotional state is expected to produce a negative or pessimistic judgment of an ambiguous stimulus, whereas a positive emotional state produces a positive or optimistic judgment of the same ambiguous stimulus. Measuring an animal's emotional state or mood is relevant in both animal welfare research and biomedical research. This is reflected in the increasing use of JBTs in both research areas. We discuss the different implementations of JBTs with animals, with a focus on their potential as an accurate measure of emotional state. JBTs have been successfully applied to a very broad range of species, using many different types of testing equipment and experimental protocols. However, further validation of this test is deemed necessary. For example, the often extensive training period required for successful judgment bias testing remains a possible factor confounding results. Also, the issue of ambiguous stimuli losing their ambiguity with repeated testing requires additional attention. Possible improvements are suggested to further develop the JBTs in both animal welfare and biomedical research.