Project

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Formation and function of Drosophila taste circuits

Applicant Sprecher Simon
Number 136307
Funding scheme Sinergia
Research institution Département de Biologie Faculté des Sciences Université de Fribourg
Institution of higher education University of Fribourg - FR
Main discipline Embryology, Developmental Biology
Start/End 01.01.2012 - 30.11.2015
Approved amount 1'887'241.00
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All Disciplines (2)

Discipline
Embryology, Developmental Biology
Neurophysiology and Brain Research

Lay Summary (English)

Lead
Lay summary

Neural circuits transform sensory information in the external world into abstract patterns of electrical activity in the brain to induce adaptive behavioural responses. The innate nature of many animal behaviours argues that their underlying circuits are specified by precise genetic programmes acting during development. Research in several model systems has contributed substantial insights into the genetic specification of neuron types, the mechanisms of neural guidance and wiring specificity, and the contribution of individual neural populations to specific animal behaviours. However, our understanding of the organisation of complete neural circuits – from sensory input to motor output – is very limited. This lack of knowledge has obscured a view of how genetic programmes may act coordinately in distinct neural lineages to specify a functionally integrated circuit. We investigate the genetic basis of the formation and function of neural circuits through comprehensive characterisation of gustatory circuitry in the fruit fly, Drosophila melanogaster. Drosophila taste circuits offer a number of advantageous properties to tackle this fundamental problem. First, this sensory modality is relatively simple: as in vertebrates, gustatory perception in Drosophila comprises a limited number of sensory pathways underling distinct classes of tastants (e.g. sweet, bitter, salty). Second, taste stimuli evoke robust behavioural responses - notably extension or retraction of the proboscis (the main feeding organ of the fly) - that also reveal evidence of more sophisticated processing properties, such as adaptation and sensory integration. Third, the circuitry is likely quite shallow from sensory input to motoneuron output, with proboscis extension probably controlled by a limited number of interneurons residing entirely with the primary gustatory center, a part of the suboesophageal ganglion (SOG). Finally, the Drosophila model offers a powerful combination of genetic tools for precise spatial and temporal manipulation of gene and neuronal function, and access to high-resolution cellular imaging, physiological analysis and quantitative behavioural assessment. Together, these offer unparalleled potential for dissection of the development, structure and function of neural circuits.

Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
An expression atlas of variant ionotropic glutamate receptors identifies a molecular basis of carbonation sensing
Sánchez-Alcañiz Juan Antonio, Silbering Ana Florencia, Croset Vincent, Zappia Giovanna, Sivasubramaniam Anantha Krishna, Abuin Liliane, Sahai Saumya Yashmohini, Münch Daniel, Steck Kathrin, Auer Thomas O., Cruchet Steeve, Neagu-Maier G. Larisa, Sprecher Simon G., Ribeiro Carlos, Yapici Nilay, Benton Richard (2018), An expression atlas of variant ionotropic glutamate receptors identifies a molecular basis of carbonation sensing, in Nature Communications, 9(1), 4252-4252.
Structure and development of the subesophageal zone of the Drosophila brain. II. Sensory compartments
Kendroud Sarah, Bohra Ali A., Kuert Philipp A., Nguyen Bao, Guillermin Oriane, Sprecher Simon G., Reichert Heinrich, VijayRaghavan Krishnaswamy, Hartenstein Volker (2018), Structure and development of the subesophageal zone of the Drosophila brain. II. Sensory compartments, in Journal of Comparative Neurology, 526(1), 33-58.
Organization of the Drosophila larval visual circuit
Larderet Ivan, Fritsch Pauline MJ, Gendre Nanae, Neagu-Maier G Larisa, Fetter Richard D, Schneider-Mizell Casey M, Truman James W, Zlatic Marta, Cardona Albert, Sprecher Simon G (2017), Organization of the Drosophila larval visual circuit, in eLife, 6, 1.
Functional genomics identifies regulators of the phototransduction machinery in the Drosophila larval eye and adult ocelli
Mishra Abhishek Kumar, Bargmann Bastiaan O.R., Tsachaki Maria, Fritsch Cornelia, Sprecher Simon G. (2016), Functional genomics identifies regulators of the phototransduction machinery in the Drosophila larval eye and adult ocelli, in Developmental Biology, 410(2), 164-177.
Multimodal stimulus coding by a gustatory sensory neuron in Drosophila larvae.
Lena van Giesen, Luis Hernandez-Nunez, Sophie Delasoie-Baranek, Martino Colombo, Philippe Renauld, Rémy Bruggmann, Richard Benton, Aravinthan Samuel, Simon Sprecher (2016), Multimodal stimulus coding by a gustatory sensory neuron in Drosophila larvae., in Nature Communications, 1.
Characterization of tailless functions during Drosophila optic lobe formation
Guillermin Oriane, Perruchoud Benjamin, Sprecher Simon G., Egger Boris (2015), Characterization of tailless functions during Drosophila optic lobe formation, in Developmental Biology, 405(2), 202-213.
Potency of Transgenic Effectors for Neurogenetic Manipulation in Drosophila Larvae
Pauls Dennis, von Essen Alina, Lyutova Radostina, van Giesen Lena, Rosner Ronny, Wegener Christian, Sprecher Simon G. (2015), Potency of Transgenic Effectors for Neurogenetic Manipulation in Drosophila Larvae, in Genetics, 199(1), 25-37.
Neuroblast lineage identification and lineage-specific Hox gene action during postembryonic development of the subesophageal ganglion in the Drosophila central brain
Kuert Philipp (2014), Neuroblast lineage identification and lineage-specific Hox gene action during postembryonic development of the subesophageal ganglion in the Drosophila central brain, in Developmental Biology , 390(2014), 102-115.

Collaboration

Group / person Country
Types of collaboration
Rolf Urbach, University of Mainz Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results

Associated projects

Number Title Start Funding scheme
180316 Neural Processing of Distinct Prediction Errors: Theory, Mechanisms & Interventions 01.09.2018 Sinergia

Abstract

Neural circuits transform sensory information in the external world into abstract patterns of electrical activity in the brain to induce adaptive behavioural responses. The innate nature of many animal behaviours argues that their underlying circuits are specified by precise genetic programmes acting during development. Research in several model systems has contributed substantial insights into the genetic specification of neuron types, the mechanisms of neural guidance and wiring specificity, and the contribution of individual neural populations to specific animal behaviours. However, our understanding of the organisation of complete neural circuits - from sensory input to motor output - is very limited. This lack of knowledge has obscured a view of how genetic programmes may act coordinately in distinct neural lineages to specify a functionally integrated circuit. This Sinergia project aims to address the genetic basis of the formation and function of neural circuits through comprehensive characterisation of gustatory circuitry in the fruit fly, Drosophila melanogaster. Drosophila taste circuits offer a number of advantageous properties to tackle this fundamental problem. First, this sensory modality is relatively simple: as in vertebrates, gustatory perception in Drosophila comprises a limited number of sensory pathways underling distinct classes of tastants (e.g. sweet, bitter, salty). Second, taste stimuli evoke robust behavioural responses - notably extension or retraction of the proboscis (the main feeding organ of the fly) - that also reveal evidence of more sophisticated processing properties, such as adaptation and sensory integration. Third, the circuitry is likely quite shallow from sensory input to motoneuron output, with proboscis extension probably controlled by a limited number of interneurons residing entirely with the primary gustatory center, a part of the suboesophageal ganglion (SOG). Finally, the Drosophila model offers a powerful combination of genetic tools for precise spatial and temporal manipulation of gene and neuronal function, and access to high resolution cellular imaging, physiological analysis and quantitative behavioural assessment. Together, these offer unparalleled potential for dissection of the development, structure and function of neural circuits. The project has four specific aims:1.Generating genetic tools for the analysis of gustatory circuitry.2.Identification and mapping the elements of gustatory circuitry.3.Structural identification and physiological characterisation of circuit elements and synaptic connectivity.4.Genetic analysis of developmental specification and functional organisation in the taste circuit: towards a "developmental algorithm" for neural circuit formation.Together these aims will provide a comprehensive anatomical and functional map of gustatory processing pathways and insights into the cellular origins and genetic mechanisms by which individual circuit elements arise and wire together during development. The scale and interdisciplinary demands of the research aims necessitate a collaborative approach, and the success of the project will depend critically on the wide-ranging and complementary expertise of the participating groups, in developmental biology (Sprecher, Hartenstein, Reichert), high-resolution neuroanatomy (Hartenstein, Reichert, Pielage), molecular genetics (Pielage, Benton, Sprecher), neural physiology (Benton, Pielage) and behavioural analysis (Benton, Sprecher).
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