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

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

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.Acknowledgements: We thank the staff at MRC-CFM, particularly Faye Peters and Sebastian Merritt who assisted with data collection.National Centre for the Replacement, Refinement and Reduction of Animals in Research; funder-id: http://dx.doi.org/10.13039/501100000849; Grant(s): grantNC/L000539/1Liverpool John Moores University; funder-id: http://dx.doi.org/10.13039/501100004144; Grant(s): PhD studentshi

Microplastics disrupt hermit crab shell selection

Microplastics (plastics < 5 mm) are a potential threat to marine biodiversity. However, the effects of microplastic pollution on animal behaviour and cognition are poorly understood. We used shell selection in common European hermit crabs (Pagurus bernhardus) as a model to test whether microplastic exposure impacts the essential survival behaviours of contacting, investigating and entering an optimal shell. We kept 64 female hermit crabs in tanks containing either polyethylene spheres (n = 35) or no plastic (n = 29) for 5 days. We then transferred subjects into suboptimal shells and placed them in an observation tank with an optimal alternative shell. Plastic-exposed hermit crabs showed impaired shell selection: they were less likely than controls to contact optimal shells or enter them. They also took longer to contact and enter the optimal shell. Plastic exposure did not affect time spent investigating the optimal shell. These results indicate that microplastics impair cognition (information-gathering and processing), disrupting an essential survival behaviour in hermit crabs

Optimism and pasture access in dairy cows

Allowing dairy cattle to access pasture can promote natural behaviour and improve their health. However, the psychological benefits are poorly understood. We compared a cognitive indicator of emotion in cattle either with or without pasture access. In a crossover experiment, 29 Holstein–Friesian dairy cows had 18 days of overnight pasture access and 18 days of full-time indoor housing. To assess emotional wellbeing, we tested cows on a spatial judgement bias task. Subjects learnt to approach a rewarded bucket location, but not approach another, unrewarded bucket location. We then presented cows with three “probe” buckets intermediate between the trained locations. Approaching the probes reflected an expectation of reward under ambiguity—an “optimistic” judgement bias, suggesting positive emotional states. We analysed the data using linear mixed-effects models. There were no treatment differences in latency to approach the probe buckets, but cows approached the known rewarded bucket slower when they had pasture access than when they were indoors full-time. Our results indicate that, compared to cattle housed indoors, cattle with pasture access display less anticipatory behaviour towards a known reward. This reduced reward anticipation suggests that pasture is a more rewarding environment, which may induce more positive emotional states than full-time housing

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 behavioural classification of morphs towards ‘fear’ following adaptation to neutral compared to adaptation to fear with a non-significant trend towards 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 post-stimulus onset, in the high but not the low anxiety group following adaptation to neutral compared to fear. In addition, as the size of the behavioural 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 late positive potential deflection

Early differences in auditory processing relate to Autism Spectrum Disorder traits in infants with Neurofibromatosis Type I

Abstract: Background: Sensory modulation difficulties are common in children with conditions such as Autism Spectrum Disorder (ASD) and could contribute to other social and non-social symptoms. Positing a causal role for sensory processing differences requires observing atypical sensory reactivity prior to the emergence of other symptoms, which can be achieved through prospective studies. Methods: In this longitudinal study, we examined auditory repetition suppression and change detection at 5 and 10 months in infants with and without Neurofibromatosis Type 1 (NF1), a condition associated with higher likelihood of developing ASD. Results: In typically developing infants, suppression to vowel repetition and enhanced responses to vowel/pitch change decreased with age over posterior regions, becoming more frontally specific; age-related change was diminished in the NF1 group. Whilst both groups detected changes in vowel and pitch, the NF1 group were largely slower to show a differentiated neural response. Auditory responses did not relate to later language, but were related to later ASD traits. Conclusions: These findings represent the first demonstration of atypical brain responses to sounds in infants with NF1 and suggest they may relate to the likelihood of later ASD