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Specifically, rodent models have shown that exposure to either a single severe (acute) stressor, or several mild (chronic) stressful experiences are sufficient in inducing a depressogenic effect 23, 24. Stressful life events have been implicated in the aetiology of depression in both humans and animals 21, 22. How an animal responds to both punishment and reward offers a way of accessing their enduring negative affective states: whilst anxiety and depression can both be characterized by greater expectation of punishment, depression is also associated with a reduced expectation of reward 20.
HEDONIC METHOD FULL
Whilst previous studies investigating the effects of handling method on mouse welfare have measured the animals’ behaviour towards aversive experiences or punishments (such as being picked up by a handler or being placed in a novel test environment 13, 14, 15), measuring responses to positive experiences and rewards (hedonic responses) are also important for understanding the full impact of handling methods on the affective state of an animal 17, 18, 19. Here, we extend previous work on handling methods to test if being handled by the tail or with a tunnel can affect the hedonic responses of mice towards a rewarding stimulus. However, despite the evidence that tail handling can impair welfare and scientific data collection, it remains the main method used to handle mice and other more refined methods such as tunnel handling have yet to be widely implemented across research institutions. In addition, tail handling can reduce performance in cognitive tests, for example it has been shown to reduce the engagement of mice with a novel mouse odour in a habituation task, resulting in the impairment of the subsequent dishabituation test 15.
HEDONIC METHOD PLUS
The standard practice of handling laboratory mice using their tails has been shown to increase anxiety compared to being handled with a tunnel or by cupping mice on the open hand 13, 14, 15: tunnel handled mice spend more time voluntarily interacting with a handler, and show less anxiety-related behaviour in standardised behavioural tests of anxiety such as the elevated plus maze 13, 14, 15. However, more recently, it has been proposed that the handling technique used by researchers and laboratory staff influences both the welfare of mice, and the data obtained from behavioural studies 13, 14, 15, 16. This revealed that small cage sizes, lack of environmental enrichment, room temperatures and isolation can all negatively impact on mouse welfare, producing measurable changes in behaviour, physiology or affective state 9, 10, 11, 12. Much early work examined the housing in which mice are kept. Consequently, understanding the experiences of mice used in research is of significant importance in order to be able to provide evidence-based improvements to housing and husbandry that will bring welfare benefits to a large number of animals, and ensure that empirical findings are robust 3, 8. Mice are the most widely used species in biomedical research globally in 2016 they were used in 73% of all procedures in the UK alone 7. Laboratory environments can negatively impact on the behaviour, physiology, health and welfare of animals 1, 2, 3, 4 and considerable effort is made to regulate and improve the welfare of animals used in research laboratories around the world 5, 6. Our findings have significant implications for the welfare of laboratory mice as well as the design and interpretation of scientific studies, particularly those investigating or involving reward. We found that tail handled mice showed more anhedonic responses in both measures compared to tunnel handled mice, indicative of a decreased responsiveness to reward and potentially a more depressive-like state. Anhedonia is a core symptom of clinical depression, and is measured in rodents by assessing how they consume a sucrose solution: depressed mice consume less sucrose and the size of their licking bouts when drinking (their ‘lick cluster sizes’) also tend to be smaller. In this study, we provide the first evidence that tail handling also reduces mice’s responses to reward. However, despite clear negative effects on mice’s behaviour, tunnel handling has yet to be widely implemented. Recent studies have identified that the standard practice of handling laboratory mice by their tails increases behaviours indicative of anxiety, which can be overcome by handling mice using a tunnel. Consequently, it is important to refine laboratory procedures and practices to ensure high standards of welfare and scientific data quality. Mice are the most widely used model species for drug discovery and scientific research.