Sex-Specific Effect of Recalled Parenting on Affective and Cognitive Empathy in Adulthood

Previous research has demonstrated the influence of parenting on the development of children’s empathy. However, few studies have considered the impact of parents on empathy in adulthood, specific components of empathy, or the importance of parent and child biological sex. In the present study, 226 participants (71 men) completed online versions of the Parental Bonding Instrument (Parker et al. British Journal of Medical Psychology, 52, 1–10 1979), Empathy Quotient (Baron-Cohen and Wheelwright Journal of Autism and Developmental Disorders, 34, 163–175 2004), and Interpersonal Reactivity Index (Davis JSAS Catalog of Selected Documents in Psychology, 10, 85 1980). Paternal care and overprotection influenced affective empathy in men, whilst maternal overprotection predicted affective empathy in women. Further, maternal care related to cognitive empathy in men, whilst none of the parental care variables related to cognitive empathy in women. Findings are discussed in relation to sex differences in childhood parenting experiences on adult cognitive and affective empathy

Pasture Access Affects Behavioral Indicators of Wellbeing in Dairy Cows

Dairy cows are increasingly housed indoors, either year-round or for long stretches over the winter and around parturition. This may create health and welfare issues. In cattle, lying and walking are highly motivated, and herds synchronize lying behavior when they have comfortable surfaces and little competition for space. Lying and walking activity can, therefore, indicate good welfare. Using a repeated measures crossover design, we gave 29 Holstein–Friesian dairy cows 18 days of overnight pasture access (PAS treatment) and 18 days of indoor housing (PEN treatment). Accelerometers recorded their lying and locomotory behavior. We measured behavioral synchrony with Fleiss’ Kappa and analyzed the accelerometry data using linear mixed models. Compared to the PEN treatment, the PAS treatment had longer overnight lying durations (χ21 = 27.51, p < 0.001), fewer lying bouts (χ21 = 22.53, p < 0.001), longer lying bouts (χ21 = 25.53, p < 0.001), and fewer transitions up or down (χ21 = 16.83, p < 0.001). Herd lying behavior was also more synchronous at pasture (χ21 = 230.25, p < 0.001). In addition, nightly step counts were higher in the PAS treatment than the PEN treatment (χ21 = 2946.31, p < 0.001). These results suggest pasture access improves dairy cow welfare by increasing comfort, reducing competition and boredom, and facilitating motivated behavior

Cognitive bias in a non-human primate: husbandry procedures influence cognitive indicators of psychological well-being in captive rhesus macaques

The measurement of 'cognitive bias' has recently emerged as a powerful tool for assessing animal welfare. Cognitive bias was initially, and widely, studied in humans, and describes the way in which particular emotions are associated with biases in information processing. People suffering from clinical levels of anxiety or depression, for example, interpret ambiguous events more negatively than do non-anxious or non-depressed people. Development of methods for use with non-human animals has revealed similar biases in several species of mammals and birds, and one invertebrate. However, cognitive bias has not been previously explored in any species of non-human primate, despite specific concerns raised about the welfare of these animals in captivity. Here, we describe a touchscreen-based cognitive-bias task developed for use with captive rhesus macaques (Macaca mulatta). Monkeys were initially trained on a 'Go/No-Go' operant task, in which they learned to touch one of two lines that differed in size in order to receive a reward (food), and to desist from touching the other line to avoid a mildly aversive stimulus (delay to the next trial and white noise). In testing sessions, the monkeys were presented with lines of intermediate size. We measured whether touchscreen responses to these ambiguous stimuli were affected by husbandry procedures (environmental enrichment, and a statutory health check involving restraint and ketamine hydrochloride injection) presumed to induce positive and negative shifts in affective state, respectively. Monkeys made fewer responses to ambiguous stimuli post health check compared to during the phase of enrichment suggesting greater expectation of negative outcomes following the health check compared to during enrichment. Shifts in affective state following standard husbandry procedures may therefore be associated with changes in information processing similar to those demonstrated in anxious and depressed humans, and in a number of other taxa

Emotion evaluation and response slowing in a non-human primate: New directions for cognitive bias measures of animal welfare

The cognitive bias model of animal welfare assessment is informed by studies with humans demonstrating that the interaction between emotion and cognition can be detected using laboratory tasks. A limitation of cognitive bias tasks is the amount of training required by animals prior to testing. A potential solution is to use biologically relevant stimuli that trigger innate emotional responses. Here; we develop a new method to assess emotion in rhesus macaques; informed byparadigms used with humans: emotional Stroop; visual cueing and; in particular; response slowing. In humans; performance on a simple cognitive task can become impaired when emotional distractor content is displayed. Importantly; responses become slower in anxious individuals in the presence of mild threat; a pattern not seen in non-anxious individuals; who are able to effectively process and disengage from the distractor. Here; we present a proof-of-concept study; demonstrating that rhesus macaques show slowing of responses in a simple touch-screen task when emotional content is introduced; but only when they had recently experienced a presumably stressful veterinary inspection. Our results indicate the presence of a subtle “cognitive freeze” response; the measurement of which may provide a means of identifying negative shifts in emotion in animals

Evaluating Mood Changes in Response to Anthropogenic Noise with a Response-Slowing Task in Three Species of Zoo-housed Primates

In the zoo environment, anthropogenic noise is common as sound levels fluctuate due to visitors, construction, habitat design, and special events. In this study, changes in the mood of three species of zoo-housed primates in response to a loud annual event were evaluated with the response-slowing paradigm. In this paradigm, animals experiencing anxiety slow responses on simple cognitive tasks when emotional content is displayed. Following a previously validated approach, we measured latencies to touch potentially threatening (conspecific faces with directed gaze) and non-threatening (conspecific faces with averted gaze) images overlaid on a grey square, relative to neutral control images (grey squares only) on a touchscreen. In Experiment 1, four Japanese macaques (Macaca fuscata) were tested in two conditions: during a baseline (non-stressful) period and opportunistically during three days during which loud jets frequently flew overhead. Results indicated a significant effect of condition, with an increase in latency to touch images of conspecific faces relative to control images during the days of the loud event. In Experiment 2, chimpanzees (Pan troglodytes, n = 4) and western lowland gorillas (Gorilla gorilla gorilla, n = 2) were tested during the same loud event following a similar methodology. The results revealed subtle changes across conditions; however, this was likely driven by the apes increasing their response speed to face stimuli relative to control stimuli over time (habituation). These findings suggest that the macaques, but not the apes, underwent detectable affective changes during the loud event. With additional development, this relatively simple paradigm may be an effective and feasible way to evaluate real-time changes in the mood of zoo-housed animals

A deep transfer learning model for head pose estimation in rhesus macaques during cognitive tasks: towards a nonrestraint noninvasive 3Rs approach

Head orientation is a measure of attention used in behavioral psychological research with non-human primates. It is used across a broad range of disciplines and settings, from the field to the laboratory. Field methods are time consuming with risk of coding bias and visibility issues with free-ranging animals. Laboratory methods may require restraint and use of invasive procedures. Automated systems to measure head orientation in unrestrained animals, that are robust to partial occlusion of the head, would improve coding efficiency and accuracy and provide 3Rs animal welfare benefits. We present a free-to-use deep transfer learning model for non-invasive head pose estimation in unrestrained Macaca mulatta taking part in cognitive experiments. Monkeys housed in social groups were filmed viewing two conspecific face stimuli presented on either side of a video camera. Video frames were manually annotated for three head positions relative to the video camera: ‘left’, ‘center’ and ‘right’. The dataset (total = 8135 images from 26 monkeys) was partitioned into training and testing datasets using a leave-k-out strategy, so that 70% of the images were used in training and 30% were used in testing. We used the VGG16, VGG19, InceptionV3 and Resnet50 as base models to train the proposed head pose classifier. We achieved model accuracy up to 93%. The head pose estimation model presented here will be of use across contexts ranging from field-based playback experiments to assessment of welfare in zoo and clinical veterinary settings and refinement of neuroscience research practices. Model code with instructions is provided

Individual Variation in Dietary Wariness Is Predicted by Head Color in a Specialist Feeder, the Gouldian Finch

Shifts in resource availability due to environmental change are increasingly confronting animals with unfamiliar food types. Species that can rapidly accept new food types may be better adapted to ecological change. Intuitively, dietary generalists are expected to accept new food types when resources change, while dietary specialists would be more averse to adopting novel food. However, most studies investigating changes in dietary breadth focus on generalist species and do not delve into potential individual predictors of dietary wariness and the social factors modulating these responses. We investigated dietary wariness in the Gouldian finch, a dietary specialist, that is expected to avoid novel food. This species occurs in two main head colors (red, black), which signal personality in other contexts. We measured their initial neophobic responses (approach attempts before first feed and latency to first feed) and willingness to incorporate novel food into their diet (frequency of feeding on novel food after first feed). Birds were tested in same-sex pairs in same and different head color pairings balanced across experiments 1 and 2. Familiar and novel food (familiar food dyed) were presented simultaneously across 5 days for 3 h, each. Gouldian finches fed on the familiar food first demonstrating food neophobia, and these latencies were repeatable. Birds made more approach attempts before feeding on novel than familiar food, particularly red-headed birds in experiment 1 and when partnered with a black-headed bird. Individuals consistently differed in their rate of incorporation of novel food, with clear differences between head colors; red-headed birds increased their feeding visits to novel food across experimentation equaling their familiar food intake by day five, while black-headed birds continually favored familiar food. Results suggest consistent among individual differences in response to novel food with red-headed birds being adventurous consumers and black-headed birds dietary conservatives. The differences in food acceptance aligned with responses to novel environments on the individual level (found in an earlier study) providing individuals with an adaptive combination of novelty responses across contexts in line with potential differences in movement patterns. Taken together, these novelty responses could aid in population persistence when faced with environmental changes

Pasture access and eye temperature in dairy cows

Pasture access can benefit dairy cows’ behavior, health, and welfare, but herds are increasingly housed indoors full-time. Recent infrared thermal-imaging (thermography) studies suggest that higher eye temperatures may be a physiological indicator of chronic stress. We, therefore, hypothesized that, compared to cows with pasture access, cows housed indoors full-time would have higher eye temperatures. In a two-phase crossover experiment, 29 Holstein-Friesian dairy cows experienced 18 days of overnight pasture access and 18 days of full-time indoor housing. We measured each animal’s eye temperature 16 times (eight/phase). During Phase One, cows with pasture access had higher eye temperatures than cows housed indoors full-time (contrary to our hypothesis). However, during Phase Two, cows with pasture access had lower eye temperatures than cows housed indoors full-time. It is, therefore, unclear whether eye temperature reflected disparities in dairy cow welfare between different housing treatments

Genetic polymorphisms in the serotonin, dopamine and opioid pathways influence social attention in rhesus macaques (Macaca mulatta)

Behaviour has a significant heritable component; however, unpicking the variants of interest in the neural circuits and molecular pathways that underpin these has proven difficult. Here, we present a comprehensive analysis of the relationship between known and new candidate genes from identified pathways and key behaviours for survival in 109 adult rhesus macaques (Macaca mulatta). Eight genes involved in emotion were analysed for variation at a total of nine loci. Genetic data were then correlated with cognitive and observational measures of behaviour associated with wellbeing and survival using MCMC-based Bayesian GLMM in R, to account for relatedness within the macaque population. For four loci the variants genotyped were length polymorphisms (SLC6A4 5-hydroxytryptamine transporter length-polymorphic repeat (5-HTTLPR), SLC6A4 STin polymorphism, Tryptophan 5- hydroxylase 2 (TPH2) and Monoamine oxidase A (MAOA)) whilst for the other five (5- hydroxytryptamine receptor 2A (HTR2A), Dopamine Receptor D4 (DRD4), Oxytocin receptor (OXTR), Arginine vasopressin receptor 1A (AVPR1a), Opioid receptor mu(μ) 1 (OPRM1)) SNPs were analysed. STin genotype, DRD4 haplotype and OXTR haplotype were significantly associated with the cognitive and observational measures of behaviour associated with wellbeing and survival. Genotype for 5-HTTLPR, STin and AVPR1a, and haplotype for HTR2A, DRD4 and OXTR were significantly associated with the duration of behaviours including fear and anxiety. Understanding the biological underpinnings of individual variation in negative emotion (e.g., fear and anxiety), together with their impact on social behaviour (e.g., social attention including vigilance for threat) has application for managing primate populations in the wild and captivity, as well as potential translational application for understanding of the genetic basis of emotions in humans