Candidate Neural Substrates for Off-Edge Motion Detection in Drosophila

Abstract

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

Subcellular mapping of dendritic activity in optic flow processing neurons

“…A comparable spatial displacement could also be found for the Tm1/Tm2 and the Tm2/Tm9 input pairs on the dendrites of T5. However, information about the corresponding projection of T5 onto the lobula plate is missing [52]. On the other hand, a potential molecular mechanism for the multiplicative stage of the Reichardt detector has been proposed for this circuit: Tm1, Tm2 and Tm9 all have a cholinergic phenotype [45,52], and T5 expresses both nicotinic and muscarinic acetylcholine receptors.…”

“…Recent experiments suggest that while the excitation is likely Excitatory transmission from T4/T5 to the lobula plate is cholinergic [52,64], and sensed by nicotinic acetylcholine receptors on the dendrites of VS cells [65].…”

“…The OFF pathway, on the other hand, leads from L2 via Tm1, Tm2, and Tm4 to T5. In addition, T5 receives synaptic input from L3 via Tm9 [52]. Within the OFF pathway, L2, L4 and Tm2 form a cholinergic microcircuit, with the two reciprocally connected L2 and L4 both projecting onto Tm2 [45].…”

“…On the other hand, a potential molecular mechanism for the multiplicative stage of the Reichardt detector has been proposed for this circuit: Tm1, Tm2 and Tm9 all have a cholinergic phenotype [45,52], and T5 expresses both nicotinic and muscarinic acetylcholine receptors. Since the inputs of Tm1/Tm2 and Tm2/Tm9 are spatially segregated on T5 dendrites, this might allow for the implementation of a direct and a delay line and a multiplicative interaction between them, if nicotinic and muscarinic receptors are also asymmetrically expressed on T5 dendrites [52].…”

Analysing visual behaviour in Drosophila Dscam2 mutants using optimised optomotor and operant control assays

“…These pathways are potentially critical for the processing of delayed and non-delayed input channels of the EMD. Mi1 and Tm3 provide input to T4 (Takemura et al, 2013) and Tm1 and Tm2 provide input to T5 (Shinomiya et al, 2014). T4 and T5 are found in the lobula complex and through neuronal silencing and electrophysiological experiments in Drosophila it has been found that they respond selectively to moving light edges and dark edges respectively (Maisak et al, 2013) and provide input to the LPTCs in a directionally selective manner (Douglass & Strausfeld, 1995, Douglass & Strausfeld, 1996, Schnell et al, 2012, Strausfeld & Lee, 1991.…”