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

Repeatable glucocorticoid expression is associated with behavioural syndromes in males but not females in a wild primate

Behavioural syndromes are a well-established phenomenon in human and non-human animal behavioural ecology. However, the mechanisms that lead to correlations among behaviours and individual consistency in their expression at the apparent expense of behavioural plasticity remain unclear. The ‘state-dependent’ hypothesis posits that inter-individual variation in behaviour arises from inter-individual variation in state and that the relative stability of these states within an individual leads to consistency of behaviour. The endocrine stress response, in part mediated by glucocorticoids (GCs), is a proposed behavioural syndrome-associated state as GC levels are linked to an individual’s behavioural responses to stressors. In this study, in wild Barbary macaques (Macaca sylvanus), consistent inter-individual differences were observed in both sexes for GC activity (faecal glucocorticoid, fGC concentrations), but not GC variation (coefficient of variation in fGC concentrations). The expression of the behavioural syndrome ‘Excitability’ (characterized by the frequencies of brief affiliation or aggressive interactions) was related to GC activity in males but not in females; more ‘excitable’ males had lower GC activity. There was no relationship in females between any of the behavioural syndromes and GC activity, nor in either sex with GC variation. The negative relationship between GC activity and Excitability in males provides some support for GC expression as a behavioural syndrome-generating state under the state-dependent framework. The absence of this relationship in females highlights that state-behavioural syndrome associations may not be generalizable within a species and that broader sex differences in state need to be considered for understanding the emergence and maintenance of behavioural syndromes