Neuronal Circuitry of Olfactory Memory in Drosophila
Keywords
Drosophila, larva, mushroom bodies, calyx, olfaction, circuitry, calcium imaging
Research interests
Organisms with brains can discriminate with high specificity among an enormous range of sensory stimuli – humans even have neurons that respond to individual celebrities! The initial representation of sensory stimuli is broad and distributed across many channels but transformed into highly specific and sparse representations in the higher brain. To study this process in a simple system with powerful genetic tools, I am interested in the circuitry of odour discrimination and olfactory memory formation in Drosophila larvae, which are capable of discrimination and learning, but with many fewer neurons than humans.
We have therefore generated a sensory map of odor specificities for the antennal lobe (the first olfactory centre) and the mushroom body (MB) calyx (a secondary olfactory center essential for memory), using the simple larval olfactory system as a model. Imaging of larval brains using genetically encoded calcium indicators reveals the maps of olfactory information in both olfactory centres, with only a limited spread of activity as information passes through the circuitry. This movie shows a single glomerulus active bilaterally in the MB calyx, upon odor stimulation of larvae that have only a single functional olfactory receptor.
While studying how this process is controlled, we found that a single inhibitory neuron, the larval APL, feeds back from the MB output to the MB calyx, providing a mechanism that favours selective responses of MB neurons. We also found that octopaminergic (equivalent to mammalian noradrenergic) neurons innervate the MB calyx, and impair behavioural odour discrimination during learning.
Using a combination of connectomics, targeted neuronal imaging, optogenetics, and behaviour, we are now interested in the following questions:
- What pathways regulate activity of octopaminergic neurons?
- What are the roles of other output pathways from the calyx?
For a talk on my work for a non-specialist audience, see Pavlov’s Maggots!
Click on the thumbnails below to view movies [also linked in-text]:
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| Map of sensory innervation of larval antennal lobe glomeruli [Quicktime movie] |
Map of sensory neuron representations in larval mushroom body calyx [Quicktime movie] |
Activity in the calyx by olfactory stimulation of a single sensory neuron [Quicktime movie] |
5 key publications
- McLachlan, A.D., Wong, J.Y.H., Wan, B.A., O'Kane, C.J., Montagnese, M., Zhang, S.W., Masuda-Nakagawa, L.M. (2018). Octopaminergic neurons have multiple targets in Drosophila larval mushroom body calyx and regulate behavioral odor discrimination. BioRxiv doi:10.1101/295659
- Masuda-Nakagawa, L.M., Ito, K., Awasaki, T. and O’Kane, C.J. (2014) A single GABAergic neuron mediates feedback of odor-evoked signals in the mushroom body of larval Drosophila. Frontiers in Neural Circuits 8: 35. PMCID: PMC3988396 A summary of this paper is available HERE
- Masuda-Nakagawa, L.M., Awasaki, T., Ito, K., and O’Kane, C.J. (2010) Targeting expression to projection neurons that innervated specific mushroom body calyx and antennal lobe glomeruli in larval Drosophila. Gene Expr Patts 10: 328. PMID: 20659588
- Masuda-Nakagawa, L.M., Gendre, N., O’Kane, C.J., and Stocker, R.F. (2009) Localized olfactory representation in mushroom bodies of Drosophila larvae. Proc. Natl. Acad. Sci. USA 106: 10314-10319. PMID: 19502424
- Masuda-Nakagawa, L.M., Tanaka, N.K., and O’Kane, C.J. (2005) Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila. Proc. Natl. Acad. Sci. USA 102: 19027-19032. PMID: 163957192
>> Full list of publications on PubMed
Collaborators
Connectomics: Albert Cardona
Larval brain: Jim Truman
Page updated 5 June 2018