Early-life adversity and adult cognition: the starling as an experimental model.

Lead Research Organisation: Newcastle University
Department Name: Institute of Neuroscience

Abstract

People who experience a harsh environment in early life - for example, low birthweight, family poverty or family disruption - are more likely to experience depression, addictions and behavioural problems years later when they are adults. This suggests that harsh early conditions induce a cognitive style involving increased pessimism and impulsivity. The human evidence for such effects is necessarily correlational. To show experimentally that there is a causal relationship, an animal model is required.

In this project, we will develop a novel animal model for studying the effects of early-life conditions on adult cognition, using European starlings. Starlings have many advantages; they are long-lived, wild animals, for whom cognitive measures in the laboratory have already been developed. Most importantly, we can experimentally manipulate the harshness of the early environment in a natural setting, by either reducing the number of chicks in a nest to 2, or increasing to 7. We will create 32 enlarged and 32 reduced nests at farms in Northumberland, and take one chick from each into the laboratory, where we will use established cognitive tasks to examine pessimism and impulsivity. These tasks involve the animal having to interpret an ambiguous stimulus as either positive or negative (for pessimism), and having to choose between immediate and deferred rewards (for impulsivity). We will also examine the extent to which a positive current environment can compensate for harsh conditions in early-life, by housing half of our birds in barren and half in enriched conditions during the testing phase. In addition, we will use a number of biological measures to explore the mechanisms underlying the impact of early-life conditions on adult phenotype. These are growth profile, responsivity of the stress hormone corticosterone, oxidative stress and telomere length. Each of these has been implicated in how early events impact on adults, in humans as well as other animals.

This study will constitute the first experimental evidence for an impact of early-life events on adult pessimism and impulsivity, and will begin to elucidate the mechanisms involved. The results have important implications for understanding the causes of the excess burden of depression, addictions and conduct disorder in deprived communities, and will help understand the extent to which a positive adult environment can mitigate the effects of early-life environment.

Technical Summary

Exposure to early-life adversity is correlated with a range of psychological problems in adult humans, including affective disorders and addictions. We hypothesise that the common cognitive mechanisms underlying many of these effects are increased pessimism and impulsivity. In this project we aim to show experimentally that there is a causal relationship between early-life adversity and increased pessimism and impulsivity. We will develop a novel animal model using European starlings for studying the effects of early-life conditions on adult cognition. Starlings have the advantage of being long-lived, wild animals, for which measures of pessimism and impulsivity have already been developed. Importantly, we can manipulate the harshness of the early environment in the wild by a brood size manipulation. We will create 32 enlarged and 32 reduced broods, and, at fledging, take one chick from each nest into the lab, where we will examine pessimism (using a judgement bias task) and impulsivity (using a delayed reinforcement choice task). We will also examine the effects of perceived threat in the current environment by housing half the birds in barren and half in enriched cages during the testing phase. In addition, we will measure a number of biological variables to explore the mechanisms underlying the impact of brood size on adult phenotype. These include growth profile, corticosterone levels (baseline and response to acute capture-restraint stress), oxidative stress and telomere length. Each of these has been implicated in how early events impact adults in humans and birds. Our results will constitute the first experimental evidence for an impact of early-life events on adult pessimism and impulsivity, and will begin to elucidate the mechanisms involved. Our results will have implications for understanding the causes of the excess burden of depression and addiction in deprived communities, and the role of the adult environment in these effects.

Planned Impact

Several communities of scientific researchers will benefit from the proposed project, as outlined in Academic Beneficiaries above. In addition, it will have broader benefits for society, through its relevance to human psychiatric disorders, and through its implications for the study of animal welfare.

In recent years, there has been increased focus by governments on the psychological wellbeing of their citizens, and the social discrepancies in pessimism and impulsivity account for a significant fraction of the social variation in the burden of conditions such as depression and conduct disorder. Thus, having direct causal evidence on the impact of early-life environment on pessimism and impulsivity would help policy-makers, and charitable organisations, decide about the allocation of resources towards interventions which improve children's very early environments, rather than other kinds of interventions. Thus, the knowledge created here has potential to impact on public health policy, and, ultimately, the psychological wellbeing of society as a whole. To facilitate this, we propose to write a review article of the evidence from avian behavioural ecology for the impact of early-life environment on adult phenotype, including but not limited to the brain (see Pathways to Impact).

From the animal welfare side, the central problem in animal welfare is knowing when animals' wellbeing is compromised and when it is not. The measures this grant helps to develop, such as cognitive bias, telomere length, and impulsivity, will be added to the armamentarium of researchers, policy-makers, and welfare charities, to aid in the evidence-based resolution of welfare questions. We propose to write a synthetic article targeted at the welfare community to spread knowledge about these measures and their utility (see Pathways to Impact).

The aim of this project is to create fundamental basic knowledge concerning the impact of developmental history on adult cognition. Thus, the wider societal impacts described above will not be realised within the lifetime of the grant, but rather through the cumulative long-term impact of having a solid experimental model of these processes, published in peer-reviewed scientific papers, and available for other researchers to build upon.

Publications


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Bateson M (2014) Humans are not fooled by size illusions in attractiveness judgements. in Evolution and human behavior : official journal of the Human Behavior and Evolution Society
Bateson M (2016) Optimistic and pessimistic biases: a primer for behavioural ecologists in Current Opinion in Behavioral Sciences
Bateson M (2016) Cumulative stress in research animals: Telomere attrition as a biomarker in a welfare context? in BioEssays : news and reviews in molecular, cellular and developmental biology
 
Description In a series of studies, we have shown that adversity experienced early in life can have subtle but lasting effects on adult health and behaviour in starlings. These effects include loss of telomeres (a genetic marker linked to life expectancy), reduced flying abilities, more impulsive decision-making, and changes in eating behaviour. These patterns are relevant to understanding the childhood origins of health and psychological problems in humans.

We have found that developmental effects and current environment are often additive in their effects on the adult behavioural phenotype.

A pattern that is emerging from multiple experiments is that developmental telomere attrition is often a better predictor of adult phenotype (both behavioural and physiological) than the developmental manipulation applied to the animals.
Exploitation Route Having established the starling as a model for understanding the consequences of early-life adversity, it will now be possible to use it to investigate a number of topics, including critical periods for being affected by early conditions, and the degree to which the effects of early-life adversity are reversible later.
Sectors Agriculture, Food and Drink,Healthcare
URL https://www.staff.ncl.ac.uk/daniel.nettle/
 
Description Several of our findings showing how early-life experience can affect adult phenotype have received coverage in the local and national media.
First Year Of Impact 2013
Sector Education,Other
Impact Types Societal
 
Description BBSRC studentship
Amount £190,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom of Great Britain & Northern Ireland (UK)
Start 10/2013 
End 09/2017
 
Description ERC Advanced Grant to Daniel Nettle
Amount £1,600,000 (GBP)
Funding ID COMSTAR 666669 
Organisation European Research Council (ERC) 
Sector Public
Country European Union (EU)
Start 10/2015 
End 09/2020
 
Title Starling model of early-life adversity 
Description Our research has demonstrated the feasibility of using the European starling as a model for understanding the physiological and psychological consequences of early-life adversity in long-lived organisms. The results have considerable relevance to human health. Our papers have provided clear methods for manipulating early experience by cross-fostering of sibling pairs, and for measuring key outcome traits in the birds once they have reached adulthood. 
Type Of Material Model of mechanisms or symptoms - non-mammalian in vivo 
Year Produced 2013 
Provided To Others? Yes  
Impact None as yet. 
 
Description Collaboration with Karen Spencer 
Organisation University of St Andrews
Department School of Psychology St Andrews
Country United Kingdom of Great Britain & Northern Ireland (UK) 
Sector Academic/University 
PI Contribution The birds are reared, housed and studied at Newcastle University under the direction of Bateson, Nettle and their team, who also take responsibility for outputs and management of the grant.
Collaborator Contribution Dr. Spencer provides hormonal analysis of samples from the birds, as well as intellectual input into the design of studies.
Impact None of the papers as yet published under this grant involve an endocrine component, and so the St. Andrews team has not yet been involved in the papers, but this may change in coming years.
Start Year 2009
 
Description Collaboration with Pat Monaghan 
Organisation University of Glasgow
Country United Kingdom of Great Britain & Northern Ireland (UK) 
Sector Academic/University 
PI Contribution The BBRSC grant is held jointly between Newcastle University, Glasgow University and St. Andrews University. The birds are reared, kept and studied at Newcastle University by Bateson, Nettle and their team.
Collaborator Contribution Blood samples are sent from Newcastle to Glasgow, where they are analysed for telomere length and for oxidative stress. Monaghan also provides intellectual input into the grant in terms of design of future studies and measures.
Impact Several papers (detailed elsewhere) are joint with Monaghan and her colleagues from Glasgow.
Start Year 2011