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Lifespan behavioural and neural resilience in a social insect.

ABSTRACT: Analyses of senescence in social species are important to understanding how group living influences the evolution of ageing in society members. Social insects exhibit remarkable lifespan polyphenisms and division of labour, presenting excellent opportunities to test hypotheses concerning ageing and behaviour. Senescence patterns in other taxa suggest that behavioural performance in ageing workers would decrease in association with declining brain functions. Using the ant Pheidole dentata as a model, we found that 120-day-old minor workers, having completed 86% of their laboratory lifespan, showed no decrease in sensorimotor functions underscoring complex tasks such as alloparenting and foraging. Collaterally, we found no age-associated increases in apoptosis in functionally specialized brain compartments or decreases in synaptic densities in the mushroom bodies, regions associated with integrative processing. Furthermore, brain titres of serotonin and dopamine--neuromodulators that could negatively impact behaviour through age-related declines--increased in old workers. Unimpaired task performance appears to be based on the maintenance of brain functions supporting olfaction and motor coordination independent of age. Our study is the first to comprehensively assess lifespan task performance and its neurobiological correlates and identify constancy in behavioural performance and the absence of significant age-related neural declines.

SUBMITTER: Giraldo YM

PROVIDER: S-EPMC4721105 | biostudies-literature | 2016 Jan

REPOSITORIES: biostudies-literature

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Lifespan behavioural and neural resilience in a social insect.

Giraldo Ysabel Milton YM Kamhi J Frances JF Fourcassié Vincent V Moreau Mathieu M Robson Simon K A SK Rusakov Adina A Wimberly Lindsey L Diloreto Alexandria A Kordek Adrianna A Traniello James F A JF

Proceedings. Biological sciences 20160101 1822

Analyses of senescence in social species are important to understanding how group living influences the evolution of ageing in society members. Social insects exhibit remarkable lifespan polyphenisms and division of labour, presenting excellent opportunities to test hypotheses concerning ageing and behaviour. Senescence patterns in other taxa suggest that behavioural performance in ageing workers would decrease in association with declining brain functions. Using the ant Pheidole dentata as a mo ...[more]

PMID: 26740614

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Project description:ObjectiveRecent findings suggest that diminished processing of positive contextual information about others during interactions may contribute to social impairment in the schizophrenia spectrum. This could be due to general social context processing deficits or specific biases against positive information. We studied the impact of positive and negative social contextual information during social interactions using functional neuroimaging and probed whether these neural mechanisms were associated with real-life social functioning in schizophrenia spectrum disorders.MethodsPatients with a schizophrenia spectrum disorder (N = 23) and controls disorder (N = 25) played three multi-round trust games during functional magnetic resonance imaging scanning, with no, positive and negative information about the counterpart's trustworthiness, while all counterparts were programmed to behave trustworthy. The main outcome variable was the height of the shared amount in the trust game, i.e. investment, representing an indication of trust. The first investment in the game was considered to be basic trust, since no behavioural feedback was given yet. We performed region-of-interest analyses and examined the association with real-life social functioning using the experience sampling method.ResultsSocial contextual information had no effect on patients' first investments, whereas controls made the lowest investment after negative and the highest investments after positive contextual information was provided. Over trials, patients decreased investments, suggesting reduced social reward learning, whereas controls increased investments in response to behavioural feedback in the negative context. Patients engaged the dorsolateral prefrontal cortex less than controls during context presentation and showed reduced activity within the caudate during repayments. In patients, lower investments were associated with more time spent alone and social exclusion and lower caudate activation was marginally significantly associated with higher perceived social exclusion.ConclusionThe failure to adapt trust to positive and negative social contexts suggests that patients have a general insensitivity to prior social information, indicating top-down processing impairments. In addition, patients show reduced sensitivity to social reward, i.e. bottom-up processing deficits. Moreover, lower trust and lower neural activation were related to lower real-life social functioning. Together, these findings indicate that improving trust and social interactions in schizophrenia spectrum needs a multi-faceted approach that targets both mechanisms.

Project description:Non-technical summaryOur analysis shows that the framing of social vulnerability is shaped by a narrow definition of resilience, focusing on post-disaster return and recovery responses. This perspective does not account for the dynamism and non-stationarity of social-ecological systems (SES) which is becoming increasingly important in the face of accelerating environmental change. Incorporating social-ecological resilience into social vulnerability analysis can improve coastal governance by accounting for adaptation and transformation, as well as scale and cross-scale interactions.Technical summarySocial vulnerability analysis has been unable to deliver outcomes that reflect the reality of vulnerability and its consequences in an era characterised by accelerating environmental change. In this work, we used critical discourse analysis and key informant interviews to understand different framings of social vulnerability in coastal governance and management, globally and in New Zealand. We found that the framing of system vulnerability could vary depending on the definition of resilience adopted, which has critical ramifications for coastal governance of linked systems of humans and nature. We found that the framing of social vulnerability in coastal governance is mainly influenced by engineering, community and disaster resilience, focusing on return and recovery governance responses to environmental change (e.g. hurricanes, wildfires). Instead, we suggest a novel perspective based on social-ecological resilience, which more accurately reflects the dynamics of linked systems of humans and nature (SES). This revised perspective, general vulnerability, accounts for the dynamics of Earth's systems across various spatial and temporal scales in the face of accelerating environmental change. Accounting for social-ecological resilience and its core aspects (i.e. panarchy, adaptation and transformation) is essential for informing coastal governance of SES (Do we adapt? or Do we transform the SES?).Social media summarySocial-ecological resilience is essential for social vulnerability analysis in the face of accelerating environmental change.

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Lifespan behavioural and neural resilience in a social insect.

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Lifespan behavioural and neural resilience in a social insect.

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