Team
Team manager: Devaud Jean-Marc
Presentation
Our objective is the integrative study of how various life experiences influence behavioural responses and brain function. More specifically, we ask how exposure to social interactions (e.g. competition, cooperation, reproduction) or to other environmental factors (e.g. food sources, stress factors) shapes cognitive performances. We seek to unravel the neural and genetic bases of such physiological or pathological effects of experience on behavior, and their possible interactions with age (development, ageing).
We address these questions in two insect model species: the honey bee Apis mellifera and the fruitfly Drosophila melanogaster, for which detailed descriptions of brain anatomy and genome are available. Studying species exhibiting different levels of social complexities allows us to consider aspects of behavioural and brain plasticity in a social context. We also have dedicated projects involving comparative approaches with other species, including humans.
Our multidisciplinary approach is poised at the interface between cognitive neuroscience, behavioural genetics, system neuroscience and experimental psychology. We use and develop state-of the-art techniques spanning from behavioral observations and precise assessment of individuals’ cognitive performances, neuroanatomy and functional imaging of the underlying brain regions and neural circuits, as well as genetic or pharmacological manipulations targeting the involved signaling pathways.
Project 1
Honey bee workers undergo continuous maturation of their brain and learning abilities over their lifetime, in relationship with their capacity to take different roles in the colony as they age – a neural and cognitive maturation that does not follow a fully fixed developmental program. On the one hand, it can be modulated by social signals contributing to adapt individual behaviours to colony needs. On the other hand, they may be disturbed if the individual is exposed to a stressor. How does individual experience of environmental or social stimuli affect brain maturation, cognitive abilities and sensitivity to stress ?
We use olfactory learning tasks involving the resolution of ambiguities, such as reversal learning, as a major readout of cognitive maturation and behavioural flexibility. We have already shown that the capacity to reversal learning requires early exposure to the hive environment, and is modulated by foraging experience. Such environmental influences contribute to shape the neural circuits in specific brain centers (the mushroom bodies) whose function is necessary for such a complex learning task.
We thus address the following questions:
– Which environmental factors (e.g. in-hive and/or floral odorants, light) shape brain and cognitive maturation, and do they do so at specific moments of adult life?
– How does chronic or acute exposure to stressors modulate mushroom development and/or cognitive capacity? In particular, how is learning performance impacted by exposure to sublethal levels of anthropogenic stressors (e.g. pollutants?)
– In turn, how does the capacity to respond to stress vary with age and/or individual experience?
– To which extent do social status (e.g. nurse, forager…) or season determine the learning performance and sensitivity to stress?
– Do honey bees and solitary bees differ in their levels of cognitive flexibility?
– Which are the neural populations and circuits involved in the regulation of these behavioural responses?
– What are the dynamics and level of plasticity of the signaling pathways identified as key regulators of stress response (e.g. allatostatins) and reversal learning (e.g. GABA)?
– Can we improve resilience to stress in honey bees?
Collaborations : R. Jeanson & C. Rampon (Toulouse), J. Carcaud & J.-C. Sandoz (Gif-sur-Yvette), M. Goubault & Ch. Lécureuil (Tours), M. Nouvian (Constance), C. Groh & W. Rössler (Wurtzbourg)
Project 2
Understanding how sensory cues from a dynamic environment are processed and translated into appropriate behaviors is a central question in neuroscience. Aggression, an innate behavior observed across species, is essential for resource acquisition, self-defense, and establishing social hierarchies. However, it is energetically costly as it involves a range of actions from threats to physical confrontations. While aggression is typically context-dependent, a small subset of individuals display dysregulated aggression, including 3-7% of humans leading to significant societal issues. Aggression is thus critical for animal survival but requires fine-tuned regulation by inhibitory mechanisms to prevent escalation. Our project seeks to investigate the fundamental mechanisms and neural circuits that support the regulation of appropriate aggressive behavior.
To tackle these fundamental questions, we employ the fruit flies, Drosophila melanogaster as a model organism, and use genetic manipulation, multiple behavioral assays and in vivo calcium imaging to answer the following questions:
– What are the neuronal circuits in the central brain that govern aggression?
– What are the underlying fundamental mechanisms?
– What are sensory inputs crucial to drive correct aggressive behavioral responses?
– How signals are transmitted to motor neurons to generate behavioral actions?
– To which extent internal and external factors influence the expression of this behavior?
Project 3
The brain processes social information through direct and indirect learning. Direct learning involves personal experience, while indirect learning, for example observational learning, involves learning from others. Mate choice is a crucial decision impacting an organism’s fitness. It can be learned through personal experience or by observing others. Observational learning, or mate-copying, allows individuals to learn from the choices of others, leading to preferences for similar traits. Based on our well-established paradigm (Figure X), we will identify and characterize the neurons involved in this social learning. We will also study how mate-copying can influence population structure in a semi-natural condition. By combining neurobiological and ecological approaches, we aim to gain a comprehensive understanding of this social learning behavior.
Figure : A typical mate-copying experiment in D. melanogaster for green versus pink males.
After a demonstration phase where an observer female witnesses a green male copulating with another female, the observer female will choose between new pink and green males.
Here 0% represents cases when the 2 male phenotypes were chosen randomly (i.e., in 50% of the trials). The observer female will choose the green male, the male trait chosen by the first female.
Project 4
The biological or cultural origin of our sophisticated mathematical skills is still debated. While most characteristics of our number representation are shared by other Vertebrates, it is difficult to arbitrate between an inherited ancestral faculty or convergent mechanisms. The evolutionary distance with insects offers the best opportunity to compare numerical systems that evolved independently. Building on the pioneered evidence of insect numerical skills, our project explores the mechanisms of numerical processing in insect with a comparative approach from Vertebrates. We aim to characterise the properties of the insect number sense at a behavioural level by designing cognitive protocols aiming to test key features of the Vertebrate system: e.g. a dual system for small and large number and a cross-modal number representation. The brain areas responsible of the insect’s sense of number will be evidenced both using bees and drosophila as a first decisive step to identify the neuronal correlates. Finally, information gained from these objectives will feed computational models reconciling for the first time modelling of the cognitive sophistication of insects while considering perception and brain architecture and connectivity constraints. The proposed research program will thus offer timely decisive elements for a better understanding on the physiological and ecological constraints for numerical cognitive faculties to emerge.
Figure : A honeybee has to choose the picture with the lowest number of shape in order to collect a drop of sucrose reward.
– Monchanin C, Drujont E, Le Roux G, Lösel PD, Barron AB, Devaud JM, Elger A, Lihoreau M (2024) Environmental exposure to metallic pollution impairs honey bee brain development and cognition. J Haz Mat 465, 133218 10.1016/j.jhazmat.2023.133218
– Sánchez-Morales A., Gigoux V, Matsoukas MT, Perez-Benito L, Fourmy D, Alibes R, Busqué F, Cordomí A, Devaud JM (2022) Reduction of stress responses in honey bees by synthetic ligands targeting an allatostatin receptor. Sci Rep 12, 167160 10.1038/s41598-022-20978-y
– Prunier A, Trannoy S (2024) Learning from fights: Males’ social dominance status impact reproductive success in Drosophila melanogaster. PLoS One 19(3):e0299839. 10.1371/journal.pone.0299839.
– Legros J, Tang G, Gautrais J, Fernandez MP, Trannoy S (2021) Long-term dietary restriction leads to development of alternative fighting strategies. (2021) Front Behav Neurosci 14;14:599676. 10.3389/fnbeh.2020.599676
– Finke V, Scheiner R, Giurfa M, Avarguès-Weber A (2023) Individual consistency in the learning abilities of honey bees: cognitive specialization within sensory and reinforcement modalities. Anim Cogn 26(3), 909-928. 10.1007/s10071-022-01741-2
– Avarguès-Weber A, Finke V, Nagy M, Szabó T, d’Amaro D, Dyer AG, Fiser J (2020) Different mechanisms underlie implicit visual statistical learning in honey bees and humans. Proc Natl Acad Sci 201919387. doi:10.1073/pnas.1919387117
– Muria A, Musso PY, Durrieu M, Portugal FR, Ronsin B, Gordon MD, Jeanson R, Isabel G (2021). Social facilitation of long-lasting memory is mediated by CO2 in Drosophila. Current Biology, 31(10) 2065-2074. doi.org/10.1016/j.cub.2021.02.044
– Nöbel S, Danchin E, Isabel G (2023) Mate copying requires the coincidence detector Rutabaga in the mushroom bodies of Drosophila melanogaster. i-Science, 26(9): 107682. doi.org/10.1016/j.isci.2023.107682
