Neural processing of context-dependent innate behavior

Project Information

FlyContext

Grant agreement ID: 637472

DOI

10.3030/637472

Project closed

EC signature date 13 February 2015

Start date 1 July 2015

End date 30 June 2021

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 497 600,00

EU contribution

€ 1 497 600,00

Coordinated by

TECHNISCHE UNIVERSITAET MUENCHEN
Germany

Periodic Reporting for period 4 - FlyContext (Neural processing of context-dependent innate behavior)

Reporting period: 2020-01-01 to 2021-06-30

Summary of the context and overall objectives of the project

Animals constantly interact with other organisms in their environment. These include conspecifics, members of other animal species, but also plants and unicellular organisms. Nervous systems have evolved to enable animals to integrate, process, remember and express behaviors at appropriate times in the right context. Chemicals produced by food sources, mating partners, hazards and even the organism’s own microbiome are indisputably the most important cues for interactions between organisms of essentially all, even the simplest of species. Accordingly, chemosensory systems show an extremely high degree of conservation from receptor molecule up to the wiring of the nervous system.
The goal of the FlyContext research program was to understand how animals detect, process and use external and internal chemosensory information to survive and reproduce in highly dynamic and competitive environments. Specifically, we aimed to uncover:
(i) which chemical cues animals use to find food or avoid danger
(ii) how these cues induce appropriate behaviour depending on the organism’s need and context
(iii) how interactions between animal and environment evolve over time
To this end, we combined the genetic toolbox of the fly with state-of-the-art tools of neurobiology, microscopy and behavioral ethology. Ultimately, we believe that our findings in the fly contribute to the understanding of human health and behavior and help to decipher how brain and body interact to maintain long-term health and well-being.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

Perceptions and decisions depend on sensory impressions, but also on past experiences and the internal state of an animal. Behavior is therefore very adaptive and flexible. Which signals and neural networks allow the communication between brain and body? And how do they modulate behavior? In this project, we studied these questions on the example of the senses of smell and taste, the most important modalities in food-related decisions and preferences. Specifically, we wanted to understand how chemosensory information is processed by the brain to guide decision-making and how physiology and metabolic needs such as hunger influence neuronal processes and cognitive function. To this end, we were using an interdisciplinary approach combining molecular biology, genetics, electrophysiology, in vivo multiphoton functional imaging and state-of-the-art behavioral analysis in the animal model Drosophila melanogaster.
The project was divided into three main workpackages (WP). The goal of WP1 was to identify the neural circuit mechanisms underpinning hunger state-dependent changes in chemosensory preference and choice behavior. In several publications, we showed that the mushroom body, the learning center of the fly, played a crucial role in foraging behavior and decision-making in hungry animals. In particular, we showed that dopaminergic neurons carry information regarding the valence of odors in a hunger state-dependent manner and thereby influence goal-directed behavior. In WP2, we concentrated on the role of reproductive state in chemosensory choices of female flies. We published several papers showing that mating modulates taste and odor processing at multiple stages in chemosensory processing -from sensory neurons to the two higher olfactory brain centers of insects. Moreover, we found that dopaminergic neurons played an important role in conveying mating state to these higher brain centers and thereby strongly impacted on chemosensory choices. Finally, in WP3, we explored the impact of pathogen infection on chemosensory processing and behavior. In a recent publication, we showed that flies lastingly adapt their feeding behavior using their mushroom body when exposed to food contaminated with pathogenic bacteria. Our data suggested that ingested pathogens activate the innate immune system which then communicates the presence of pathogens through specific neural circuits to ultimately adapt feeding behavior.


Overview of results and their dissemination:
1. Selected publications:
• Kobler J, Rodriguez FJ, Petcu I, Grunwald Kadow IC (2020). Current Biology 28:S0960-9822(20)31353-1
• K.P. Siju, Stih V, Aimon S, Gjorgjieva J, Portugues P, Grunwald Kadow IC (2020). Current Biology 30(11):2104-2115.
• Sayin S, De Backer JF, Wosniack ME, Lewis L, Siju KP, Frisch LM, Schlegel P, Edmondson-Stait A, Sharifi N, Fisher CB, Calle-Schuler S, Lauritzen S, Bock D, Costa M, Jefferis GSXE, Gjorgjieva J, Grunwald Kadow IC (2019). Neuron 104, 544–558
• Hussain, A, Pooryasin, A, Zhang, M, Loschek, LF, La Fortezza, M, Friedrich, AB, Blais, CM, Üçpunar, HK, Yépez, YA, Lehmann, M, Gompel, N, Gagneur, J, Sigrist, SJ and Grunwald Kadow IC (2018). eLife 2018;7:e32018.
• Hussain A*, Zhang M*, Üçpunar HK, Svensson T, Quillery E, Gompel N, Ignell R, Grunwald Kadow IC (2016). PLoS Biology 14:e1002454. doi:10.1371
• Hussain A*, Üçpunar HK*, Zhang M, Loschek LF, Grunwald Kadow IC (2016). PLoS Biology 14:e1002455. doi: 10.1371

2. Science outreach:
• Initiator and co-organizer of the public seminar series ‘TUM@Freising – Wissenschaft erklärt für alle’
• Speaker at TEDxTUM conference 2018 ‘Conscious Reflection’, Munich, Germany
• Speaker and discussion panelist at ‘Women of TUM’ talks 2020 on the topic ‘Mot:vat:on’
• Contributed expertise and interviews to public Science shows and journals (Radio Mikro – Bayern 2, dasGehirn.info Revista SAÚDE, 3Sat nano aha, Quarks&Co, latestThinking.org Bild der Wissenschaft)

3. Scientific presentations (selected):
Plenary lecture at Neurofly 2020, Toledo, Spain
Keynote speaker at ECRO (European Chemoreception Research Organization) Conference 2020 (Dresden, Germany)
Invited seminar at King’s college, London, UK, 2019
Invited seminar at Salk Institute, San Diego, USA, 2018
‘Structure and Function of the Insect Mushroom Body’ Conference, Janelia Research Campus, Ashburn, U.S.A. 2017

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

Since becoming group leader, I consider as my greatest achievement the demonstration that insects use their mushroom body not only for learning and memory, but also to adapt their ongoing behavior to their internal and behavioral state. This finding was surprising and has since been followed up also by other groups. With the support of the ERC project grant, we have systematically expanded our repertoire of methods over the last six years and now combine in vivo whole brain imaging during behaviour, genetic manipulations and modelling to probe how state and need influence perception and decision-making. Our data acquired during the course of the ERC project show that learning mechanisms including dopaminergic neurons enable animals to adapt their behavior and decisions not only to external information and prior experience but also to their internal state. Given the steadily increasing number of people making unhealthy feeding decisions and the rise of metabolic diseases such as obesity and diabetes in our society, these findings provide a different perspective on how to prevent and treat the occurrence of such conditions.

Fly looking investigating its environment

Fly looking investigating its environment