Valence of Facial Cues Influences Sheep Learning in a Visual Discrimination Task.

Sheep are one of the most studied farm species in terms of their ability to process information from faces, but little is known about their face-based emotion recognition abilities. We investigated (a) whether sheep could use images of sheep faces taken in situation of varying valence as cues in a simultaneous discrimination task and (b) whether the valence of the situation affects their learning performance. To accomplish this, we photographed faces of sheep in three situations inducing emotional states of neutral (ruminating in the home pen) or negative valence (social isolation or aggressive interaction). Sheep (n = 35) first had to learn a discrimination task with colored cards. Animals that reached the learning criterion (n = 16) were then presented with pairs of images of the face of a single individual taken in the neutral situation and in one of the negative situations. Finally, sheep had to generalize what they had learned to new pairs of images of faces taken in the same situation, but of a different conspecific. All sheep that learned the discrimination task with colored cards reached the learning criterion with images of faces. Sheep that had to associate a negative image with a food reward learned faster than sheep that had to associate a neutral image with a reward. With the exception of sheep from the aggression-rewarded group, sheep generalized this discrimination to images of faces of different individuals. Our results suggest that sheep can perceive the emotional valence displayed on faces of conspecifics and that this valence affects learning processes.

Development of psychophysiological motoric reactivity is influenced by peripubertal pharmacological inhibition of gonadotropin releasing hormone action--results of an ovine model.

This study reports the effects of peripubertal GnRH receptor inactivation on development of psychophysiological motoric reactivity (PMR; sometimes also called emotional reactivity), plasma cortisol concentrations and the relationship between plasma cortisol and PMR in male and female sheep. The study formed part of a larger trial and utilised 46 same sex twins. One twin remained untreated (control) while the other received a subcutaneous GnRH agonist (GnRHa Goserelin-Acetate) implant every 4th week, beginning at 8 and 28 weeks of age, in males and females, respectively (different, due to sex specific age of puberty). PMR, a measure of an animals' response to social isolation, was measured over a two minute period at 8, 28 and 48 weeks of age, using a three axis accelerometer. During the test period vocalisation rate was recorded. Cortisol was assayed in blood samples collected on a single day when animals were 40 weeks of age. PMR and vocalisation rate were significantly higher in females than males at all ages tested. At 28 weeks of age (20 weeks treatment) PMR was increased in treated males to the level seen in control females, by 48 weeks of age treated males' PMR was significantly less than controls. In females, 20 weeks of GnRHa treatment (28-48 weeks of age) was not associated with differences in PMR. Cortisol concentrations were significantly higher in females than males but were not affected by treatment. Plasma cortisol concentrations were positively correlated with PMR; this relationship being driven by the treated animals in both sexes. The results demonstrate that PMR is sexually dimorphic and cortisol dependent in sheep from at least 8 weeks of age. Importantly, they also demonstrate that long-term treatment of males with a GnRH agonist results in changes in age-dependent development of PMR.

Effects of pre- and postnatal polychlorinated biphenyl exposure on emotional reactivity observed in lambs before weaning.

Humans and animals are exposed to PCBs and influences on developmental and endocrine processes are among the most pronounced effects. In the present study it was hypothesised that exposure to PCBs may interfere with sexually dimorphic behaviour. To test this hypothesis, behavioural studies in developmentally exposed sheep were conducted. Ewes were orally administered PCB 153 (98 µg/kg bw day), PCB 118 (49 µg/kg bw day) or corn oil from conception until delivery. However, because of accidental cross-contamination occurring twice causing a mixed exposure scenario in all three groups, the focus of this paper is to compare three distinct groups of lambs with different PCB levels (PCB 153 high-PCB 153 h, PCB 118 high-PCB 118 h, and low combined group-LC) rather than comparing animals exposed to single PCB congeners to those of a control group. Lambs were tested between 2 and 6 weeks of age. When LC males started the light/dark choice test in a dark box, they spent significantly more time in the dark part of the pen than LC females. This gender-related difference was not found in groups exposed to PCBs. A significant inhibitory effect on the activity level of males exposed to stress of confinement was found in the PCB 118 h group. In a high stress situation females from PCB 118 h and males from PCB 153 h were less active than their gender counterparts. The results support the hypothesis that intrauterine exposure to PCBs can alter sexually dimorphic behaviour of offspring.

Prepubertal gonadotropin-releasing hormone analog leads to exaggerated behavioral and emotional sex differences in sheep.

In mammals, sex specialization is reflected by differences in brain anatomy and function. Measurable differences are documented in reproductive behavior, cognition, and emotion. We hypothesized that gonadotropin-releasing hormone (GnRH) plays a crucial role in controlling the extent of the brain's sex specificity and that changes in GnRH action during critical periods of brain development, such as puberty, will result in altered sex-specific behavioral and physiological patterns. We blocked puberty in half of the 48 same-sex Scottish mule Texel cross sheep twins with GnRH analog (GnRHa) goserelin acetate every 3 weeks, beginning just before puberty. To determine the effects of GnRHa treatment on sex-specific behavior and emotion regulation in different social contexts, we employed the food acquisition task (FAT) and measurement of heart rate variability (HRV). ANOVA revealed significant sex and sex×treatment interaction effects, suggesting that treated males were more likely to leave their companions to acquire food than untreated, while the opposite effect was observed in females. Concordant results were seen in HRV; treated males displayed higher HRV than untreated, while the reverse pattern was found in females, as shown by significant sex and sex×treatment interaction effects. We conclude that long-term prepubertal GnRHa treatment significantly affected sex-specific brain development, which impacted emotion and behavior regulation in sheep. These results suggest that GnRH is a modulator of cognitive function in the developing brain and that the sexes are differentially affected by GnRH modulation.

Individual personality and the spatial distribution of groups of grazing animals: an example with sheep.

Impacts of individual personality on group distribution were investigated using sheep (Ovis aries) as a model. In an indoor exploration test, individuals who visited <4 (out of 6) objects in a novel environment were classified as 'shy' (n=10), and those who visited 5 or 6 objects were classified as 'bold' (n=10). Nine weeks later, using a series of groups (n=40) of either 5 shy or 5 bold sheep, we measured distribution at pasture and responses to disturbance and the approach of a human handler. When grazing undisturbed, the mean nearest neighbour distance and spread (minimum convex hull area) of shy groups were less than those of bold groups, with shy individuals moving towards one another more often. Shy groups explored a smaller area than bold groups. When disturbed, shy sheep were more likely to stop grazing and move closer together. Shy sheep kept further away from the handler and moved faster when driven. The results demonstrate a link between personality and group distribution, suggesting that our 'shy' and 'bold' individuals may occupy different positions on the shy-bold continuum documented for other species. We discuss implications for diet composition and impacts on vegetation grazed by animals with different personalities.

Prenatal and postnatal exposure to environmental pollutants in sewage sludge alters emotional reactivity and exploratory behaviour in sheep.

In order to find out whether exposure to environmental pollutants (EP) present in sewage sludge can change the behaviour of sheep, we compared the behaviour of two groups of 5-month old lambs (Ovis aries) with respect to their emotional reactivity and exploratory behaviour. One group (treated, T) comprised the offspring of ewes who had been kept throughout their lives on pastures with slightly elevated, environmental levels of pollutants, as a result of the application of sewage sludge at rates used in normal practice. The other group (control, C) were the offspring of ewes whose pastures had been treated with inorganic fertiliser. During a 1-min period in the weigh crate, T lambs were less reactive than C lambs, but vocalised more. Exploratory behaviour showed a clear sex difference, with female C lambs exploring more than male C lambs. However, this difference was not found in the T lambs, where both males and females showed high levels of exploration. This points to a demasculinising effect of exposure to higher pollutant concentrations with respect to exploratory behaviour. These observations demonstrate the need to take account of the effects of combinations of pollutants, even at very low, environmental concentrations, and further highlight the usefulness of ethotoxicology for the study of biological effects of environmental pollutants.

Effects of prenatal undernutrition on emotional reactivity and cognitive flexibility in adult sheep.

The experiment reported was designed to test two hypotheses: that prenatal undernutrition (a) increases emotional reactivity and (b) impairs cognitive flexibility in sheep. The mothers of one group were fed live weight maintenance requirements throughout pregnancy (control, C) while those of another group were fed 50% of that amount from days 1 to 95 of pregnancy and 100% from then onwards (prenatal undernutrition, PU). At 18 months of age, PU sheep were more active during restraint (P < 0.05) and approached a novel stimulus more slowly (P = 0.02). In response to a sudden stimulus, PU males and C females showed a higher initial level of locomotion compared to C males, which only gradually declined, while PU females started at a high initial rate, changing rapidly to immobility. In a T-maze, PU resulted in a shift of side preferences (laterality) from a general right-bias to neutrality in males and to a left-bias in females (P < 0.05). In the two reversal tasks, C males and PU females had a preference for one side over the other, while PU males showed no preference. In contrast to C males, PU males failed to improve their learning speed from the first to the second reversal (P < 0.05). It is concluded that PU can lead to increased emotional reactivity and changes in side preference in both sexes and impaired cognitive flexibility in males. Undernutrition during pregnancy, therefore, not only affects the welfare of the dam, but also the personality of her offspring.