Presynaptic developmental plasticity allows robust sparse wiring of the Drosophila mushroom body

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Abstract

In order to represent complex stimuli, principle neurons of associative learning regions receive combinatorial sensory inputs. Density of combinatorial innervation is theorized to determine the number of distinct stimuli that can be represented and distinguished from one another, with sparse innervation thought to optimize the complexity of representations in networks of limited size. How the convergence of combinatorial inputs to principle neurons of associative brain regions is established during development is unknown. Here, we explore the developmental patterning of sparse olfactory inputs to Kenyon cells of the Drosophila melanogaster mushroom body. By manipulating the ratio between pre- and post-synaptic cells, we find that postsynaptic Kenyon cells set convergence ratio: Kenyon cells produce fixed distributions of dendritic claws while presynaptic processes are plastic. Moreover, we show that sparse odor responses are preserved in mushroom bodies with reduced cellular repertoires, suggesting that developmental specification of convergence ratio allows functional robustness.

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Analyzed data points generated during the study are included in the figures. Source data for Figure 7 is presented in a source data file.

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Najia A Elkahlah

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Jackson A Rogow

Laboratory of Neurophysiology and Behavior, The Rockefeller University, New York, United States

Competing interests
The authors declare that no competing interests exist.
Maria Ahmed

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
E Josie Clowney

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States

For correspondence
jclowney@umich.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-9150-9464

Funding

Rita Allen Foundation (Milton Cassel Scholar)

E Josie Clowney

Alfred P. Sloan Foundation (Research Fellow in Neuroscience)

E Josie Clowney

University of Michigan (Startup Funds)

E Josie Clowney

University of Michigan (Neuroscience Scholar Award)

E Josie Clowney

Helen Hay Whitney Foundation (Simons Fellow)

E Josie Clowney

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

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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.