Pavlovian influences on learning differ between rats and mice in a counter-balanced Go/NoGo judgement bias task

Samantha Jones,Elizabeth S Paul,Peter Dayan,Emma S.J Robinson,Michael Mendl

doi:10.1016/j.bbr.2017.05.044

Samantha Jones, Elizabeth S Paul + Show 3 more

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https://doi.org/10.1016/j.bbr.2017.05.044

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Abstract

Judgement bias tests of animal affect and hence welfare assume that the animal’s responses to ambiguous stimuli, which may herald positive or negative outcomes, are under instrumental control and reflect ‘optimism’ or ‘pessimism’ about what will happen. However, Pavlovian control favours responses (e.g. approach or withdrawal) according to the valence associated with a stimulus, rather than the anticipated response outcomes. Typically, positive contexts promote action and approach whilst negative contexts promote inhibition or withdrawal. The prevalence of Go-for-reward (Go-pos) and NoGo-to-avoid-punishment (NoGo-neg) judgement bias tasks reflects this Pavlovian influence. A Pavlovian increase or decrease in activity or vigour has also been argued to accompany positive or negative affective states, and this may interfere with instrumental Go or NoGo decisions under ambiguity based on anticipated decision outcomes. One approach to these issues is to develop counter-balanced Go-pos/NoGo-neg and Go-neg/NoGo-pos tasks. Here we implement such tasks in Sprague Dawley rats and C57BL/6J mice using food and air-puff as decision outcomes. We find striking species/strain differences with rats achieving criterion performance on the Go-pos/NoGo-neg task but failing to learn the Go-neg/NoGo-pos task, in line with predictions, whilst mice do exactly the opposite. Pavlovian predispositions may thus differ between species, for example reflecting foraging and predation ecology and/or baseline activity rates. Learning failures are restricted to cues predicting a negative outcome; use of a more powerful air-puff stimulus may thus allow implementation of a fully counter-balanced task. Rats and mice achieve criterion faster than in comparable automated tasks and also show the expected generalisation of responses across ambiguous tones. A fully counter-balanced task thus offers a potentially rapidly implemented and automated method for assessing animal welfare, identifying welfare problems and areas for welfare improvement and 3Rs Refinement, and assessing the effectiveness of refinements.

Highlights

Valid translational models of affective disorders, better measures of animal welfare that allow more effective detection of welfare problems and implementation of 3Rs Refinements, and a deeper understanding of the evolutionary history and mechanistic underpinnings of affective states, all require accurate measurement of affect in animals
For the rat (Sprague Dawley) and mouse (C57BL/6J) strains used, one of the two counter-balanced contingencies in the shuttle box task was learnt but the other was not. This differed between species/strains with rat data supporting the hypothesis that Pavlovian control favours Go-pos/ NoGo-neg learning whilst mouse data supported the opposite − that it favours Go-neg/NoGo-pos learning
A deeper understanding of the learning processes mediating performance in judgement bias tasks may aid in their interpretation, and shed light on contradictory results in the literature

Summary

Introduction

Valid translational models of affective disorders, better measures of animal welfare that allow more effective detection of welfare problems and implementation of 3Rs Refinements, and a deeper understanding of the evolutionary history and mechanistic underpinnings of affective states, all require accurate measurement of affect in animals. Developed for rats [1], the generic judgement bias assay involves training animals to make one type of response (P: e.g. leverpress) to a cue predicting a positive event or reward (p: e.g. a tone of a particular frequency) in order to receive that reward (e.g. food delivery), and another type of response (N: e.g. no lever-press) to a cue predicting a negative event or punisher (n: e.g. a tone of a different frequency) in order to avoid that event (e.g. white noise) Once this discrimination is learnt, subjects receive occasional ‘ambiguous’ cues (e.g. tones in between p and n). Judgement biases may be useful indicators of the valence of an animal’s affective state even though, like all measures of animal affect, they cannot tell us whether the inferred affective state is consciously experienced in other species [53]

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