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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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
- Neuroscience
The assembly and maintenance of neural circuits is crucial for proper brain function. Although the assembly of brain circuits has been extensively studied, much less is understood about the mechanisms controlling their maintenance as animals mature. In the olfactory system, the axons of olfactory sensory neurons (OSNs) expressing the same odor receptor converge into discrete synaptic structures of the olfactory bulb (OB) called glomeruli, forming a stereotypic odor map. The OB projection neurons, called mitral and tufted cells (M/Ts), have a single dendrite that branches into a single glomerulus, where they make synapses with OSNs. We used a genetic method to progressively eliminate the vast majority of M/T cells in early postnatal mice, and observed that the assembly of the OB bulb circuits proceeded normally. However, as the animals became adults the apical dendrite of remaining M/Ts grew multiple branches that innervated several glomeruli, and OSNs expressing single odor receptors projected their axons into multiple glomeruli, disrupting the olfactory sensory map. Moreover, ablating the M/Ts in adult animals also resulted in similar structural changes in the projections of remaining M/Ts and axons from OSNs. Interestingly, the ability of these mice to detect odors was relatively preserved despite only having 1–5% of projection neurons transmitting odorant information to the brain, and having highly disrupted circuits in the OB. These results indicate that a reduced number of projection neurons does not affect the normal assembly of the olfactory circuit, but induces structural instability of the olfactory circuitry of adult animals.
