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Social experience and the establishment of behavioural syndromes - novel insights from crickets into the role of serotonin in aggression, “personality” and depression-like phenomena

Subject Area Cognitive, Systems and Behavioural Neurobiology
Term from 2018 to 2022
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 400443783
 
Final Report Year 2022

Final Report Abstract

Experiencing aggression, especially during early life, can have manifold detrimental influences on a victim’s behaviour and health in both humans and animals, but the chain of events in the brain that ultimately lead to this are largely unknown. This project uses field crickets as a model system to investigate the influence of aggressive experience on subsequent behaviour and how such effects are mediated by chemical transmitters in the brain. Adult male crickets exhibit spectacular fighting behaviour when they meet, and we have shown that an individual’s decision to persist in fighting or turn and flee is controlled largely by neurotransmitters similar or the same as those that influence aggression in mammals: octopamine (OA) the invertebrate analogue of noradrenaline, serotonin (5HT) and nitric oxide (NO). We now show that while the stress of a single defeat induces only a short phase (< 3 h) of depressed aggressiveness, this lasts for days and potentially life long after multiple intermittent defeats. This effect of chronic social defeat stress is also known in rodents, but little understood - in particular why some individuals are more resilient and other susceptible. We found that the effect in crickets is due mainly to 5HT acting via a 5HT2-like receptor: a receptor antagonist induced resilience to defeat stress, whereas elevating endogenous 5HT action by inhibiting its re-uptake, increased susceptibility. Aggression experienced during early life of cricket nymphs was also found to lead in adults to consistent inter-individual differences in behaviour - or “personality” types. Mature adults subjected to early life adversity, by raising them together with aggressive adult males, tend either to approach a novel stimuli (e.g a touch of an antenna), or turn to avoid it. In contrast, these behavioural differences were not evident in mature adults not exposed to early life adversity. However, after 6 successive fights winners all showed approach behaviour, whereas losers showed avoidance, consistently for at least 6 days subsequently. Surprisingly, the decision to approach or avoid appears to be mediated primarily if not alone by OA. An OA receptor antagonist induced approachers to become avoiders (but had no effect on avoiders), whereas an OA agonist induced avoiders to become approachers (but had no effect on approachers). Interestingly, avoiders also tended to be less aggressive, lose more fights, be less motile and less exploratory than approachers. The latter suggests the existence of a so-called proactive-reactive behavioural syndrome in crickets. Finally, in order to analyse the effects of agonistic experience on an individual’s cognitive capacity, we developed a novel method to quantify learning based on multiple behavioural features of a focal animal’s conditioned odour response using binary logistic regression. The method proved superior to standard methods using only a single behavioural predictor, and revealed a high level of inter-individual variability in learning. Contrary to our expectation, this variability did not appear to result alone from prior agonistic experience. Nonetheless, complementing similar findings in mammals, we found that defeat stress seriously impedes learning capacity. Employing two similar odours in a differential conditioning procedure in which only one is rewarded during training, we made the surprising discovery that defeat stress increased the response to the non-conditioned odour while decreasing the response to the condition odour. Furthermore, these effects appear due to activation of 5HT2 -like receptors. A receptor agonist rendered the animals resilient to defeat stress, whereas the 5HT re-uptake inhibitor fluoxetin (Prozac) induced greater susceptibility to defeat stress, while neither of these drugs influenced learning in non-stressed animals. We speculate that defeat stress leads to release of 5HT in key brain regions involved in olfactory learning, such as the mushroom bodies. Whether Prozac has similar - context selective - effects on humans that receive it to treat depression or various obsessive compulsive disorder, is to our knowledge unknown. Together our findings illustrate that behavioural individuality (“personality”), as well as correlations between different behaviours that characterise a behavioural syndrome can arise, at least in crickets, as an ultimate result of the action of neurotransmitters released during earlier agonistic experiences. Chronic defeat stress in particular has clearly subduing effects on social behaviour, motor behaviour and assertive decision making, as well severe detrimental effects on learning capacity. Our finding that this depends largely on activation of a specific 5HT receptor subtype calls for further investigations into how this forges long term changes in brain function, presumably via coupled second messengers acting to regulate protein synthesis and gene expression.

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