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Opposite Effects of Early-Life Competition and Developmental Telomere Attrition on Cognitive Biases in Juvenile European Starlings.

Bateson M, Emmerson M, Ergün G, Monaghan P, Nettle D - PLoS ONE (2015)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Centre for Behaviour & Evolution and Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom.

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.

No MeSH data available.


Related in: MedlinePlus

Effects of developmental telomere attrition on judgment bias.Latency to probe as a function of telomere attrition score. Telomere attrition score is the difference between telomere length at d4 and d55 adjusted for regression to the mean (see methods for details); negative values correspond to greater telomere loss. Data points are the mean ± 1s.d. of the ln latency to probe in the 24 judgment bias test trials with ambiguous stimuli (i.e. valences 2–4) for each bird (n = 22). The solid line shows the predicted regression line derived from the model described in the main text.
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pone.0132602.g002: Effects of developmental telomere attrition on judgment bias.Latency to probe as a function of telomere attrition score. Telomere attrition score is the difference between telomere length at d4 and d55 adjusted for regression to the mean (see methods for details); negative values correspond to greater telomere loss. Data points are the mean ± 1s.d. of the ln latency to probe in the 24 judgment bias test trials with ambiguous stimuli (i.e. valences 2–4) for each bird (n = 22). The solid line shows the predicted regression line derived from the model described in the main text.

Mentions: Since we have previously shown that number of heavier competitors at d15 predicts developmental telomere attrition in the same group of birds, we next explored whether developmental telomere attrition statistically mediates [43] the relationship between number of heavier competitors and cognitive bias established above. Developmental telomere attrition was correlated with number of heavier competitors, but not so strongly as to preclude entering both predictors into the same model and their having separate effects (r = -0.47, see Table 3). As previously, the dependent variable was latency to probe the ambiguous stimuli (logged). The fixed predictors initially included were: speed, valence (2–4), heavier competitors, the valence by heavier competitors interaction, telomere length at d4, developmental telomere attrition (D) and the valence by developmental telomere attrition interaction. Since the valence by telomere attrition interaction was not significant, we excluded this interaction from the final model for which we present parameter estimates below. Speed significantly predicted latency to probe with birds that had faster mean speeds probing POS and NEG also probing ambiguous stimuli faster (GLMM: B ± se = 0.07 ± 0.01, X2(1) = 31.53, p < 0.001). Valence also significantly predicted latency to probe with birds probing stimuli more similar to POS faster (GLMM: B ± se = -0.70 ± 0.08, X2(1) = 89.82, p < 0.001). Number of heavier competitors was not significant, but the interaction between valence and number of heavier competitors reported above remained significant (GLMM: B ± se = 0.08 ± 0.03, X2(1) = 7.94, p = 0.005). Telomere length at d4 was marginally non-significant, with birds with shorter telomeres at d4 tending to probe faster (GLMM: B ± se = 0.24 ± 0.12, X2(1) = 3.23, p = 0.072). Telomere attrition, D, significantly predicted latency to probe, with birds that had suffered greater developmental telomere attrition probing ambiguous stimuli faster (GLMM: B ± se = 0.41 ± 0.20, X2(1) = 4.02, p = 0.045; Fig 2). The fit of the model including developmental telomere attrition was better than the model containing just number of heavier competitors as a predictor when the two models were run on the same restricted data set (ΔAICc = -1.88) arguing for the retention of developmental telomere attrition in our final model of the birds’ behaviour towards ambiguous stimuli. Note that the effect of developmental telomere attrition reported here is qualitatively the same if the model is run without number of heavier competitors included (statistics not shown). We can thus conclude that number of heavier competitors and developmental telomere attrition appear to have independent and opposite effects on the birds’ relative latencies to probe ambiguous stimuli.


Opposite Effects of Early-Life Competition and Developmental Telomere Attrition on Cognitive Biases in Juvenile European Starlings.

Bateson M, Emmerson M, Ergün G, Monaghan P, Nettle D - PLoS ONE (2015)

Effects of developmental telomere attrition on judgment bias.Latency to probe as a function of telomere attrition score. Telomere attrition score is the difference between telomere length at d4 and d55 adjusted for regression to the mean (see methods for details); negative values correspond to greater telomere loss. Data points are the mean ± 1s.d. of the ln latency to probe in the 24 judgment bias test trials with ambiguous stimuli (i.e. valences 2–4) for each bird (n = 22). The solid line shows the predicted regression line derived from the model described in the main text.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4519284&req=5

pone.0132602.g002: Effects of developmental telomere attrition on judgment bias.Latency to probe as a function of telomere attrition score. Telomere attrition score is the difference between telomere length at d4 and d55 adjusted for regression to the mean (see methods for details); negative values correspond to greater telomere loss. Data points are the mean ± 1s.d. of the ln latency to probe in the 24 judgment bias test trials with ambiguous stimuli (i.e. valences 2–4) for each bird (n = 22). The solid line shows the predicted regression line derived from the model described in the main text.
Mentions: Since we have previously shown that number of heavier competitors at d15 predicts developmental telomere attrition in the same group of birds, we next explored whether developmental telomere attrition statistically mediates [43] the relationship between number of heavier competitors and cognitive bias established above. Developmental telomere attrition was correlated with number of heavier competitors, but not so strongly as to preclude entering both predictors into the same model and their having separate effects (r = -0.47, see Table 3). As previously, the dependent variable was latency to probe the ambiguous stimuli (logged). The fixed predictors initially included were: speed, valence (2–4), heavier competitors, the valence by heavier competitors interaction, telomere length at d4, developmental telomere attrition (D) and the valence by developmental telomere attrition interaction. Since the valence by telomere attrition interaction was not significant, we excluded this interaction from the final model for which we present parameter estimates below. Speed significantly predicted latency to probe with birds that had faster mean speeds probing POS and NEG also probing ambiguous stimuli faster (GLMM: B ± se = 0.07 ± 0.01, X2(1) = 31.53, p < 0.001). Valence also significantly predicted latency to probe with birds probing stimuli more similar to POS faster (GLMM: B ± se = -0.70 ± 0.08, X2(1) = 89.82, p < 0.001). Number of heavier competitors was not significant, but the interaction between valence and number of heavier competitors reported above remained significant (GLMM: B ± se = 0.08 ± 0.03, X2(1) = 7.94, p = 0.005). Telomere length at d4 was marginally non-significant, with birds with shorter telomeres at d4 tending to probe faster (GLMM: B ± se = 0.24 ± 0.12, X2(1) = 3.23, p = 0.072). Telomere attrition, D, significantly predicted latency to probe, with birds that had suffered greater developmental telomere attrition probing ambiguous stimuli faster (GLMM: B ± se = 0.41 ± 0.20, X2(1) = 4.02, p = 0.045; Fig 2). The fit of the model including developmental telomere attrition was better than the model containing just number of heavier competitors as a predictor when the two models were run on the same restricted data set (ΔAICc = -1.88) arguing for the retention of developmental telomere attrition in our final model of the birds’ behaviour towards ambiguous stimuli. Note that the effect of developmental telomere attrition reported here is qualitatively the same if the model is run without number of heavier competitors included (statistics not shown). We can thus conclude that number of heavier competitors and developmental telomere attrition appear to have independent and opposite effects on the birds’ relative latencies to probe ambiguous stimuli.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Centre for Behaviour & Evolution and Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom.

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.

No MeSH data available.


Related in: MedlinePlus