Abstract
Moods are enduring affective states that we hypothesise should be affected by an individual’s developmental experience and its current somatic state. We tested whether early-life adversity, induced by manipulating brood size, subsequently altered juvenile European starlings’ (Sturnus vulgaris) decisions in a judgment bias task designed to provide a cognitive measure of mood. We predicted that starlings from larger broods, specifically those that had experienced more nest competitors larger than themselves would exhibit reduced expectation of reward, indicative of a ‘pessimistic’, depression-like mood. We used a go/no-go task, in which 30 starlings were trained to probe a grey card disc associated with a palatable mealworm hidden underneath and avoid a different shade of grey card disc associated with a noxious quinine-injected mealworm hidden underneath. Birds’ response latencies to the trained stimuli and also to novel, ambiguous stimuli intermediate between these were subsequently tested. Birds that had experienced greater competition in the nest were faster to probe trained stimuli, and it was therefore necessary to control statistically for this difference in subsequent analyses of the birds’ responses to the ambiguous stimuli. As predicted, birds with more, larger nest competitors showed relatively longer latencies to probe ambiguous stimuli, suggesting reduced expectation of reward and a ‘pessimistic’, depression-like mood. However, birds with greater developmental telomere attrition—a measure of cellular aging associated with increased morbidity and reduced life-expectancy that we argue could be used as a measure of somatic state—showed shorter latencies to probe ambiguous stimuli. This would usually be interpreted as evidence for a more positive or ‘optimistic’ affective state. Thus, increased competition in the nest and poor current somatic state appear to have opposite effects on cognitive biases. Our results lead us to question whether increased expectation of reward when presented with ambiguous stimuli always indicates a more positive affective state. We discuss the possibility that birds in poor current somatic state may adopt a ’hungry’ cognitive phenotype that could drive behaviour commonly interpreted as ‘optimism’ in food-rewarded cognitive bias tasks.
Highlights
In humans, there is substantial epidemiological evidence that various forms of early-life adversity are associated with an increased probability of developing mood disorders such as anxiety and depression later in life [1,2,3]
The birds used in the current study originated from a designed experiment in which sibling chicks were allocated to broods of either 2 or 7 chicks, previous analyses of the effects of treatment on chick weight gain showed that whilst there were overall effects of treatment, these were being driven by loser chicks in the high-competition treatment [18]
We have argued previously that continuous measures, such as either the number of heavier competitors that a chick had on d15 [18,25] or its weight on d11 [42], are more precise indices of early-life adversity than whether a chick was in the high- or low-competition treatment
Summary
There is substantial epidemiological evidence that various forms of early-life adversity are associated with an increased probability of developing mood disorders such as anxiety and depression later in life [1,2,3]. The quality of the developmental environment is likely to influence the physical quality of the body an individual is able to develop, and this somatic state variable could influence the relative costs of response errors independent of the current environment in which an animal finds itself. We predict that it should be optimal for animals with higher punishment probabilities and/or higher vulnerabilities to set lower thresholds for responding to potential threats, with the consequence that they will exhibit an anxiety-like phenotype characterised by higher expectation of punishment in the face of ambiguous information [5]. We propose that the observed relationship between early-life adversity and subsequent negative moods could be the result of an evolved response that adapts the young animal to perform optimally given either the environment in which it expects to find itself and/or the constraints of the body it has been able to develop
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