Emily Bethell

Evidence That Emotion Mediates Social Attention in Rhesus Macaques

Background Recent work on non-human primates indicates that the allocation of social attention is mediated by characteristics of the attending animal, such as social status and genotype, as well as by the value of the target to which attention is directed. Studies of humans indicate that an individual’s emotion state also plays a crucial role in mediating their social attention; for example, individuals look for longer towards aggressive faces when they are feeling more anxious, and this bias leads to increased negative arousal and distraction from other ongoing tasks. To our knowledge, no studies have tested for an effect of emotion state on allocation of social attention in any non-human species. Methodology We presented captive adult male rhesus macaques with pairs of adult male conspecific face images - one with an aggressive expression, one with a neutral expression - and recorded gaze towards these images. Each animal was tested twice, once during a putatively stressful condition (i.e. following a veterinary health check), and once during a neutral (or potentially positive) condition (i.e. a period of environmental enrichment). Initial analyses revealed that behavioural indicators of anxiety and stress were significantly higher after the health check than during enrichment, indicating that the former caused a negative shift in emotional state. Principle Findings The macaques showed initial vigilance for aggressive faces across both conditions, but subsequent responses differed between conditions. Following the health check, initial vigilance was followed by rapid and sustained avoidance of aggressive faces. By contrast, during the period of enrichment, the macaques showed sustained attention towards the same aggressive faces. Conclusions/Significance These data provide, to our knowledge, the first evidence that shifts in emotion state mediate social attention towards and away from facial cues of emotion in a non-human animal. This work provides novel insights into the evolution of emotion-attention interactions in humans, and mechanisms of social behaviour in non-human primates, and may have important implications for understanding animal psychological wellbeing.

A “How-To” Guide for Designing Judgment Bias Studies to Assess Captive Animal Welfare

Robust methods to assess nonhuman animal emotion are essential for ensuring good welfare in captivity. Cognitive bias measures such as the judgment bias task have recently emerged as promising tools to assess animal emotion. The simple design and objective response measures make judgment bias tasks suitable for use across species and contexts. In reviewing 64 studies published to date, it emerged that (a) judgment biases have been measured in a number of mammals and birds and an invertebrate; (b) no study has tested judgment bias in any species of fish, amphibian, or reptile; and (c) no study has yet investigated judgment bias in a zoo or aquarium. This article proposes that judgment bias measures are highly suitable for use with these understudied taxa and can provide new insight into welfare in endangered species housed in zoos and aquariums, where poor welfare impacts breeding success and, ultimately, species survival. The article includes a “how-to” guide to designing judgment bias tests with recommendations for working with currently neglected “exotics” including fishes, amphibians, and reptiles.

Happy hamsters? Enrichment induces positive judgement bias for mildly (but not truly) ambiguous cues to reward and punishment in Mesocricetus auratus

Recent developments in the study of animal cognition and emotion have resulted in the ‘judgement bias’ model of animal welfare. Judgement biases describe the way in which changes in affective state are characterized by changes in information processing. In humans, anxiety and depression are characterized by increased expectation of negative events and negative interpretation of ambiguous information. Positive wellbeing is associated with enhanced expectation of positive outcomes and more positive interpretation of ambiguous information. Mood-congruent judgement biases for ambiguous information have been demonstrated in a range of animal species, with large variation in the way tests are administered and in the robustness of analyses. We highlight and address some issues using a laboratory species not previously tested: the Syrian hamster (Mesocricetus auratus). Hamsters were tested using a spatial judgement go/no-go task in enriched and unenriched housing. We included a number of controls and additional behavioural tests and applied a robust analytical approach using linear mixed effects models. Hamsters approached the ambiguous cues significantly more often when enriched than unenriched. There was no effect of enrichment on responses to the middle cue. We discuss these findings in light of mechanisms underlying processing cues to reward, punishment and true ambiguity, and the implications for the welfare of laboratory hamsters.

Adapting effects of emotional expression in anxiety: Evidence for an enhanced Late Positive Potential

An adaptation paradigm was used to investigate the influence of a previously experienced visual context on the interpretation of ambiguous emotional expressions. Affective classification of fear-neutral ambiguous expressions was performed following repeated exposure to either fearful or neutral faces. There was a shift in the behavioral classification of morphs toward “fear” following adaptation to neutral compared to adaptation to fear with a nonsignificant trend toward the high-anxiety group compared to the low being more influenced by the context. The event-related potential (ERP) data revealed a more pronounced late positive potential (LPP), beginning at ~400 ms poststimulus onset, in the high but not the low-anxiety group following adaptation to neutral compared to fear. In addition, as the size of the behavioral adaptation increased, there was a linear increase in the magnitude of the late-LPP. However, context-sensitivity effects are not restricted to trait anxiety, with similar effects observed with state anxiety and depression. These data support the proposal that negative moods are associated with increased sensitivity to visual contextual influences from top-down elaborative modulations, as reflected in an enhanced LPP deflection.

Emotion Evaluation and Response Slowing in a Non-Human Primate: New Directions for Cognitive Bias Measures of Animal Emotion?

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 by paradigms 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.

Planning your PHD

Introduction PART I: YOUR PHD IDEA - WHERE NEXT? PART II: STARTING OUT PART III: TOWARDS YOUR LITERATURE REVIEW PART IV: TOWARDS YOUR PROPOSAL PART V: WRITING YOUR PROPOSAL PART VI: THE SHAPE OF THINGS TO COME

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.

A protocol for training group-housed rhesus macaques (Macaca mulatta) to cooperate with husbandry and research procedures using positive reinforcement

Highlights • We present a protocol for station-training adult rhesus macaques in social groups of 2–9 adults.• 61/65 monkeys successfully trained to sit by individual targets.• All males trained in 2 × 15 min training sessions.• High rank females trained in 6 × 15 min sessions; low rank females: 11 × 15 min.• Dominance rank was the only predictor of time taken to train.

Celebrating 50 years of the Primate Society of Great Britain

The Primate Society of Great Britain was established in 1967 by John Napier and colleagues for the scientific study of everything related to primates. It is credit to Napier’s foresight that the Society’s 400+ members represent fields as diverse as anatomy, behaviour, cognition, conservation, ecology, evolution, physiology, neuro- and veterinary sciences and captive welfare. The 50th anniversary conference was held at the Royal Geographical Society, London, on 28th – 29th November 2017. What more prestigious way to start a 50th celebration than with a letter of congratulations from the Queen, HRH Elizabeth II? This was read out as part of the President’s opening address by Simon Bearder to the 400 delegates gathered to celebrate past achievements and look forward to the next 50 years of primatology research in the UK.

Affect-Driven Attention Biases as Animal Welfare Indicators: Review and Methods.

Simple Summary Good animal welfare requires minimizing suffering and promoting positive experiences. To achieve this, we need reliable indicators of animals’ psychological states. In humans, different moods and emotions (“affects”) are associated with changes in visual attention (“attention bias”). We review studies investigating whether attention biases are also indicators of affect in animals. Although research is limited, evidence for affect-driven attention biases has been found in several species, especially primates and livestock. These studies are discussed in relation to tasks developed for measuring attention in humans. We identify additional findings from human psychology that might be applied to animals, particularly species not studied before, and conclude that affect-driven attention bias is a promising welfare indicator. However, it may be more useful for studying responses to specific stimuli, rather than general wellbeing. With further study, we hope these findings contribute to fulfilling society’s ethical obligations towards animals. Abstract Attention bias describes the differential allocation of attention towards one stimulus compared to others. In humans, this bias can be mediated by the observer’s affective state and is implicated in the onset and maintenance of affective disorders such as anxiety. Affect-driven attention biases (ADABs) have also been identified in a few other species. Here, we review the literature on ADABs in animals and discuss their utility as welfare indicators. Despite a limited research effort, several studies have found that negative affective states modulate attention to negative (i.e., threatening) cues. ADABs influenced by positive-valence states have also been documented in animals. We discuss methods for measuring ADAB and conclude that looking time, dot-probe, and emotional spatial cueing paradigms are particularly promising. Research is needed to test them with a wider range of species, investigate attentional scope as an indicator of affect, and explore the possible causative role of attention biases in determining animal wellbeing. Finally, we argue that ADABs might not be best-utilized as indicators of general valence, but instead to reveal specific emotions, motivations, aversions, and preferences. Paying attention to the human literature could facilitate these advances.