Current Biology
Volume 24, Issue 10, 19 May 2014, Pages 1062-1070
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Article
Candidate Neural Substrates for Off-Edge Motion Detection in Drosophila

https://doi.org/10.1016/j.cub.2014.03.051Get rights and content
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Highlights

  • EM reveals synaptic inputs to T5 cells that signal motion direction in Drosophila

  • Four classes of transmedulla (Tm) interneurons relay the L2 and L3 pathways to T5

  • T5 expresses nicotinic and muscarinic receptors to integrate Tm cholinergic inputs

  • Fast nicotinic excitation and delayed muscarinic inhibition mediate two arms of EMD

Summary

Background

In the fly’s visual motion pathways, two cell types—T4 and T5—are the first known relay neurons to signal small-field direction-selective motion responses [1]. These cells then feed into large tangential cells that signal wide-field motion. Recent studies have identified two types of columnar neurons in the second neuropil, or medulla, that relay input to T4 from L1, the ON-channel neuron in the first neuropil, or lamina, thus providing a candidate substrate for the elementary motion detector (EMD) [2]. Interneurons relaying the OFF channel from L1’s partner, L2, to T5 are so far not known, however.

Results

Here we report that multiple types of transmedulla (Tm) neurons provide unexpectedly complex inputs to T5 at their terminals in the third neuropil, or lobula. From the L2 pathway, single-column input comes from Tm1 and Tm2 and multiple-column input from Tm4 cells. Additional input to T5 comes from Tm9, the medulla target of a third lamina interneuron, L3, providing a candidate substrate for L3’s combinatorial action with L2 [3]. Most numerous, Tm2 and Tm9’s input synapses are spatially segregated on T5’s dendritic arbor, providing candidate anatomical substrates for the two arms of a T5 EMD circuit; Tm1 and Tm2 provide a second. Transcript profiling indicates that T5 expresses both nicotinic and muscarinic cholinoceptors, qualifying T5 to receive cholinergic inputs from Tm9 and Tm2, which both express choline acetyltransferase (ChAT).

Conclusions

We hypothesize that T5 computes small-field motion signals by integrating multiple cholinergic Tm inputs using nicotinic and muscarinic cholinoceptors.

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