Functional and anatomical specificity in a higher olfactory centre
- MRC Laboratory of Molecular Biology, United Kingdom
- The Francis Crick Institute, United Kingdom
- University of Cambridge, United Kingdom
- Janelia Research Campus, Howard Hughes Medical Institute, United States
Abstract
Most sensory systems are organized into parallel neuronal pathways that process distinct aspects of incoming stimuli. In the insect olfactory system, second order projection neurons target both the mushroom body, required for learning, and the lateral horn (LH), proposed to mediate innate olfactory behavior. Mushroom body neurons form a sparse olfactory population code, which is not stereotyped across animals. In contrast, odor coding in the LH remains poorly understood. We combine genetic driver lines, anatomical and functional criteria to show that the Drosophila LH has ~1400 neurons and >165 cell types. Genetically labeled LHNs have stereotyped odor responses across animals and on average respond to three times more odors than single projection neurons. LHNs are better odor categorizers than projection neurons, likely due to stereotyped pooling of related inputs. Our results reveal some of the principles by which a higher processing area can extract innate behavioral significance from sensory stimuli.
Data availability
Digital skeletons for neuronal morphology and summary electrophysiological data have been provided as supplemental zip files. An interactive version of these data is available as online supplement linked from the paper. Full source data and source code are available on GitHub.
Article and author information
Author details
Alexander Shakeel Bates
Michael-John Dolan
Arian Rokkum Jamasb
Gregory SXE Jefferis
Funding
European Commission (ERC CoG 649111)
- Shahar Frechter
- Alexander Shakeel Bates
- Sina Tootoonian
- Michael-John Dolan
- James D Manton
- Gregory SXE Jefferis
Medical Research Council (U105188491)
- Shahar Frechter
- Alexander Shakeel Bates
- Michael-John Dolan
- James D Manton
- Johannes Kohl
- Gregory SXE Jefferis
Wellcome (203261/Z/16/Z)
- Arian Rokkum Jamasb
- Davi Bock
- Gregory SXE Jefferis
European Commission (ERC StG 211089)
- Shahar Frechter
- Alexander Shakeel Bates
- Sina Tootoonian
- Michael-John Dolan
- James D Manton
- Gregory SXE Jefferis
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2019, Frechter et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Neuroscience
A combination of genetic, anatomical and physiological techniques has revealed that the lateral horn, a region of the brain involved in olfaction in flies, has many more types of neurons than expected.
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- Neuroscience
- Physics of Living Systems
Neurons generate and propagate electrical pulses called action potentials which annihilate on arrival at the axon terminal. We measure the extracellular electric field generated by propagating and annihilating action potentials and find that on annihilation, action potentials expel a local discharge. The discharge at the axon terminal generates an inhomogeneous electric field that immediately influences target neurons and thus provokes ephaptic coupling. Our measurements are quantitatively verified by a powerful analytical model which reveals excitation and inhibition in target neurons, depending on position and morphology of the source-target arrangement. Our model is in full agreement with experimental findings on ephaptic coupling at the well-studied Basket cell-Purkinje cell synapse. It is able to predict ephaptic coupling for any other synaptic geometry as illustrated by a few examples.
