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

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

Emotion in animal contests

Emotions encompass cognitive and behavioural responses to reward and punishment. Using contests as a case-study, we propose that short-term emotions underpin animals' assessments, decision-making and behaviour. Equating contest assessments to emotional ‘appraisals', we describe how contestants appraise more than resource value and outcome probability. These appraisals elicit the cognition, drive and neurophysiology that governs aggressive behaviour. We discuss how recent contest outcomes induce long-term moods, which impact subsequent contest behaviour. Finally, we distinguish between integral (objectively relevant) and incidental (objectively irrelevant) emotions and moods (affective states). Unlike existing ecological models, our approach predicts that incidental events influence contest dynamics, and that contests become incidental influences themselves, potentially causing maladaptive decision-making. As affective states cross contexts, a more holistic ethology (incorporating emotions and moods) would illuminate animal cognition and behaviour

Cognitive Bias in Ambiguity Judgements:Using Computational Models to Dissect the Effects of Mild Mood Manipulation in Humans

Positive and negative moods can be treated as prior expectations over future delivery of rewards and punishments. This provides an inferential foundation for the cognitive (judgement) bias task, now widely-used for assessing affective states in non-human animals. In the task, information about affect is extracted from the optimistic or pessimistic manner in which participants resolve ambiguities in sensory input. Here, we report a novel variant of the task aimed at dissecting the effects of affect manipulations on perceptual and value computations for decision-making under ambiguity in humans. Participants were instructed to judge which way a Gabor patch (250ms presentation) was leaning. If the stimulus leant one way (e.g. left), pressing the REWard key yielded a monetary WIN whilst pressing the SAFE key failed to acquire the WIN. If it leant the other way (e.g. right), pressing the SAFE key avoided a LOSS whilst pressing the REWard key incurred the LOSS. The size (0-100 UK pence) of the offered WIN and threatened LOSS, and the ambiguity of the stimulus (vertical being completely ambiguous) were varied on a trial-by-trial basis, allowing us to investigate how decisions were affected by differing combinations of these factors. Half the subjects performed the task in a 'Pleasantly' decorated room and were given a gift (bag of sweets) prior to starting, whilst the other half were in a bare 'Unpleasant' room and were not given anything. Although these treatments had little effect on self-reported mood, they did lead to differences in decision-making. All subjects were risk averse under ambiguity, consistent with the notion of loss aversion. Analysis using a Bayesian decision model indicated that Unpleasant Room subjects were ('pessimistically') biased towards choosing the SAFE key under ambiguity, but also weighed WINS more heavily than LOSSes compared to Pleasant Room subjects. These apparently contradictory findings may be explained by the influence of affect on different processes underlying decision-making, and the task presented here offers opportunities for further dissecting such processes