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

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.

Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons

“…VT033006-GAL4 labels most PNs from the anterodrosal and lateral lineage, but not PNs from the ventral lineage or anterior paired lateral (APL) neurons like GH146-GAL4 . It is expressed in ~95 cells that innervate ~44 glomeruli which largely overlap with PNs labeled by GH146-GAL4 ( Inada et al, 2017 ; Elkahlah et al, 2020 ). In addition to PNs labeled by GH146-GAL4 and VT033006-GAL4 (we will refer to them as ‘most PNs’ hereafter), we have collected single-cell transcriptomic data using drivers that only label a small number of PN types for mapping the transcriptomic clusters to anatomically defined PN types.…”

Temporal evolution of single-cell transcriptomes ofDrosophilaolfactory projection neurons

“…VT033006-GAL4 labels most PNs from the anterodrosal and lateral lineage, but not PNs from the ventral lineage or anterior paired lateral (APL) neurons like GH146-GAL4 . It is expressed in ∼95 cells that innervate ∼44 glomeruli which largely overlap with PNs labeled by GH146-GAL4 (Inada et al, 2017; Elkahlah et al, 2020). In addition to PNs labeled by GH146-GAL4 and VT033006-GAL4 (we will refer them as ‘most PNs’ hereafter), we have collected single-cell transcriptomic data using drivers that only label a small number of PN types for mapping the transcriptomic clusters to anatomically defined PN types.…”

Complete connectomic reconstruction of olfactory projection neurons in the fly brain

“…However, PN axons in the LH arbourise in a much more diverse neuropil with a wider range of partners, making it harder to conceive of effective compensation mechanisms. It may be that a PN type's dendritic postsynapse density and its axonal presynapse density are independently regulated, most likely by their synaptic partners [29,60]. However, since glomeru-lar size positively correlates with a PN type's output synapse budget as well as the glomerular OSN count [29], it seems some global mechanism marks out individual PN types to form synapses densely or lightly at both ends.…”