Attention Bias: A novel method to assess psychological wellbeing in group-housed non-human primates

Lead Research Organisation: Liverpool John Moores University
Department Name: Natural Sciences and Psychology

Abstract

A better understanding of emotions and feelings in animals is of paramount importance to animal welfare science, but measuring psychological well-being in animals is intrinsically difficult. Existing indicators of well-being focus on indirect physiological or behavioural measures that have a number of limitations, particularly in their interpretation. Work with humans shows that psychological well-being is directly linked to biases in attention for particular types of information, and this can be measured using simple orienting paradigms. Our previous work has shown these methods are suitable for adaptation for use with animals and may provide a new and powerful set of welfare assessment tools.

In this project we will adapt, refine and validate a state-of-the-art welfare assessment tool, based on our initial work on 'attention bias' (AB) in non-human primates (Bethell et al 2012 PLoS ONE 7:e44387). In humans, AB describes the way in which people who are anxious are vigilant for threatening social information: they are faster to detect potential threats (such as an angry face), and look at such threatening material for longer than do non-anxious people. As a result, anxious individuals are over-exposed to stimuli that will reinforce their negative mood; such preferential attention to even mildly threatening information has special significance for welfare, as it is associated with vulnerability to clinical levels of anxiety, and impaired psychological wellbeing.

Previously, we successfully developed a method for assessing AB in individually housed captive rhesus macaques, by filming their gaze towards images of aggressive and neutral macaque faces. We will now adapt the original test for use with group-housed rhesus macaques at a breeding facility in the UK, and refine the method to provide an easily applied tool that can be implemented by care staff to assess psychological wellbeing in animals living in social groups. We will then validate AB as a measure of well-being using behavioural and physiological indicators of welfare and associated genetic indicators of emotion pre-disposition, and assess the extent to which individual AB scores can be used to predict responses to future stressors such as a pre-planned veterinary inspection.

This research represents a ground-breaking approach to assessment of welfare in captive animals. It directly addresses the NC3Rs objective for the refinement of the use of animals in research, through development of a powerful but easily employed tool to assess psychological wellbeing and to predict responses to future stressors. This method will facilitate improvement of welfare in research situations where use of primates is unavoidable, and enhance the lifetime experience of these animals. Psychologically healthy research animals will be physically healthier and more robust to stressors and illness, more likely to learn protocols, and provide 'cleaner' data. Once established for non-human primates, it is anticipated the assessment tools developed will be suitable for adaptation for use with a range of other taxa, including domestic pets and livestock.

Longer term, our research group is working towards adapting a new human therapeutic application - 'attention bias modification' to develop a novel intervention that will go beyond assessing psychological states to improve psychological wellbeing in captive rhesus macaques. Recent work with humans has demonstrated that, while increased vigilance towards threat leads to increased anxiety, training people to attend away from threatening stimuli leads to a reduction in anxious or depressed mood, and reduces vulnerability to anxiety following real-life stressors. A key focus of our approach is to utilise latest technological developments in hand-held computer technologies to provide the best quality widely accessible and afforadble tools for assessing and improving the welfare of captive animals.

Technical Summary

Aim: The aim of this pilot study is to contribute to the NC3Rs objective of refinement by developing and validating a state-of-the-art technological tool for assessing psychological wellbeing in captive non-human primates. This novel method focuses on quantifying attention bias - a bias in visual attention that has been linked to underlying emotional state in both humans and (recently by our research group) captive rhesus macaques.

Objectives:
1. Adapt methods we recently developed to assess attention bias in captive and free-ranging male rhesus macaques, for use with group-housed female rhesus macaques.

2. Validate attention bias as a measure of psychological state, by triangulating attention bias scores with behavioural and physiological state indicators, and genetic trait indicators of emotion and wellbeing.

3. Develop a 'quick and easy' attention bias assessment tool that can be applied widely and inexpensively by care staff, to reliably determine individual attention bias scores.

4. Assess the extent to which baseline attention bias scores predict the nature and degree of change in behavioural, physiological and attentional responses of animals to (pre-existing) stressful husbandry procedures.

Methodology: Primarily, we will film eye gaze to social stimuli for blind coding from video (Objective 1), and trial development of a flash card assessment tool using remote off-the-shelf computer eye-tracking technology (Objective 3). To address Objectives 2 and 4, we will conduct focal animal behavioural observations, enzymeimmunoassay (EIA) of salivary hormones and genetic analyses of 5-HTTLPR serial repeat polymorphisms.

Scientific opportunities: The assessment tool will provide staff at research facilities with an open access resource to maintain high standards of welfare. Breeding and supplying psychologically healthy animals to research facilities provides a grass-roots approach to improving quality of science conducted using these animals.

Planned Impact

There is a broad range of impacts from this research and specific details are given in the attached Pathways to Impact Statement.

The development of attention bias as a novel psychological assessment tool will be of use to animal care staff working with primates and other taxa, across all captive situations. At a local level, the methods will be developed in collaboration with the MRC-CFM; this facility is the primary provider of macaques for research in the UK. The methods could also be utilised by, for example, animal colony managers, zoo keepers and those involved in animal production in order to monitor and improve the welfare of their animals. Moreover, as interest grows in the emotional lives and well-being of pets and other companion animals, our work could have impact in this sector also.

Of particular value with respect to realising the benefits of this research is the development of the 'quick and easy' flash-card tool to assess attention bias in group-housed primates. The PI is in discussion with Dr Dan Witzen Hansen (IT Univeristy of Copenhagen), who already develops remote human eye-tracking systems using low-cost off-the-shelf computer technologies (e.g. tablet computers and smartphones), supported by open-access software. These technologies are designed to be affordable and easy-to-use by carers and patients with a wide range of physical disabilities, including limited motor control of head movements (e.g. as is the case in cerebral palsy), and are therefore suitable for adaptation for use with unrestrained animals, by care staff, in a range of settings. By creating a cheap, simple and accessible tool for measuring psychological well-being in non-human animals, we believe that this work will have significant and wide-ranging impact. Furthermore, by increasing staff knowledge and skills, we hope these methods will contribute towards continued improvements in standards of animal care. We will maximise this impact through a carefully developed strategy of dissemination of our work though scientific, professional and popular media to ensure that our results, together with accessible protocols and test materials, reach all relevant parties.

The potential impact of this work is not limited to non-human animals, however. As the approaches to be developed involve non-linguistic methodologies, they could also be adapted to allow the assessment of the emotional state of pre-linguistic infants and other non-linguistic people. Assessing the emotional well-being of children before they are able to express these states through language is inherently problematic. At the same time, a wide range of conditions is associated with an impaired ability - or total inability - to communicate vocally in older children, adolescents and adults, and the emotional state of such individuals is similarly challenging to monitor. This is particularly true of states like anxiety, which may not necessarily be revealed overtly via facial expressions or other such signals. We foresee that just as work with humans first inspired the approach to be developed in our study of non-human primates, so will our work provide tools that are of value for those working with people.

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