Localized inhibition in the Drosophila mushroom body

Abstract
Data availability
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Abstract

Many neurons show compartmentalized activity, in which activity does not spread readily across the cell, allowing input and output to occur locally. However, the functional implications of compartmentalized activity for the wider neural circuit are often unclear. We addressed this problem in the Drosophila mushroom body, whose principal neurons, Kenyon cells, receive feedback inhibition from a non-spiking interneuron called APL. We used local stimulation and volumetric calcium imaging to show that APL inhibits Kenyon cells’ dendrites and axons, and that both activity in APL and APL’s inhibitory effect on Kenyon cells are spatially localized (the latter somewhat less so), allowing APL to differentially inhibit different mushroom body compartments. Applying these results to the Drosophila hemibrain connectome predicts that individual Kenyon cells inhibit themselves via APL more strongly than they inhibit other individual Kenyon cells. These findings reveal how cellular physiology and detailed network anatomy can combine to influence circuit function.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1, 2, 2-supplement 1, 3, 4, 7 (Note Fig. 7 includes data from Fig. 5), 7-supplement 1, 8, 8-supplements 2&3. Custom software is available at http://github.com/aclinlab.

The following previously published data sets were used

1. Aso Y
2. Ray RP
3. Long X
4. Bushey D
5. Cichewicz K
6. Ngo TT
7. Sharp B
8. Christoforou C
9. Hu A
10. Lemire AL
11. Tillberg P
12. Hirsh J
13. Litwin-Kumar A
14. Rubin GM
(2019) Bulk RNA-seq data from the dopaminergic neurons, MB output neurons, Kenyon cells, APL and DPM neurrons in adult Drosophila
NCBI Gene Expression Omnibus, GSE139889.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE139889

Article and author information

Author details

Hoger Amin

Department of Biomedical Science, University of Sheffield, Sheffield, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-7884-4815
Anthi A Apostolopoulou

Department of Biomedical Science, University of Sheffield, Sheffield, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8174-4372
Raquel Suárez-Grimalt

Department of Biomedical Science, University of Sheffield, Sheffield, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Eleftheria Vrontou

Centre for Neural Circuits and Behaviour, University of Oxford, Oxford, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Andrew C Lin

Department of Biomedical Science, University of Sheffield, Sheffield, United Kingdom

For correspondence
andrew.lin@sheffield.ac.uk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6310-9765

Funding

H2020 European Research Council (639489)

Andrew C Lin

Biotechnology and Biological Sciences Research Council (BB/S016031/1)

Andrew C Lin

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

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.