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.
Reviewing Editor
- K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India
Version history
- Received: December 20, 2018
- Accepted: April 12, 2019
- Accepted Manuscript published: May 21, 2019 (version 1)
- Version of Record published: June 5, 2019 (version 2)
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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Functional and anatomical specificity in a higher olfactory centre
eLife 8:e44590.
https://doi.org/10.7554/eLife.44590
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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- Cell Biology
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Alternative RNA splicing is an essential and dynamic process in neuronal differentiation and synapse maturation, and dysregulation of this process has been associated with neurodegenerative diseases. Recent studies have revealed the importance of RNA-binding proteins in the regulation of neuronal splicing programs. However, the molecular mechanisms involved in the control of these splicing regulators are still unclear. Here, we show that KIS, a kinase upregulated in the developmental brain, imposes a genome-wide alteration in exon usage during neuronal differentiation in mice. KIS contains a protein-recognition domain common to spliceosomal components and phosphorylates PTBP2, counteracting the role of this splicing factor in exon exclusion. At the molecular level, phosphorylation of unstructured domains within PTBP2 causes its dissociation from two co-regulators, Matrin3 and hnRNPM, and hinders the RNA-binding capability of the complex. Furthermore, KIS and PTBP2 display strong and opposing functional interactions in synaptic spine emergence and maturation. Taken together, our data uncover a post-translational control of splicing regulators that link transcriptional and alternative exon usage programs in neuronal development.
