Two identified looming detectors in the locust: ubiquitous lateral connections among their inputs contribute to selective responses to looming objects

F Claire Rind,Julieta Sztarker,Stefan Wernitznig,Daniel Gütl,Armin Zankel,Gerd Leitinger,Peter Pölt

doi:10.1038/srep35525

Abstract

In locusts, two lobula giant movement detector neurons (LGMDs) act as looming object detectors. Their reproducible responses to looming and their ethological significance makes them models for single neuron computation. But there is no comprehensive picture of the neurons that connect directly to each LGMD. We used high-through-put serial block-face scanning-electron-microscopy to reconstruct the network of input-synapses onto the LGMDs over spatial scales ranging from single synapses and small circuits, up to dendritic branches and total excitatory input. Reconstructions reveal that many trans-medullary-afferents (TmAs) connect the eye with each LGMD, one TmA per facet per LGMD. But when a TmA synapses with an LGMD it also connects laterally with another TmA. These inter-TmA synapses are always reciprocal. Total excitatory input to the LGMD 1 and 2 comes from 131,000 and 186,000 synapses reaching densities of 3.1 and 2.6 synapses per μm2 respectively. We explored the computational consequences of reciprocal synapses between each TmA and 6 others from neighbouring columns. Since any lateral interactions between LGMD inputs have always been inhibitory we may assume these reciprocal lateral connections are most likely inhibitory. Such reciprocal inhibitory synapses increased the LGMD’s selectivity for looming over passing objects, particularly at the beginning of object approach.

Highlights

Of responses, a feature of the input organization of the LGMD 1 has been shown to be important, that of laterally spreading inhibition[18,22,23]
Four features identify it as a trans-medullary afferent cell (TmA), it has axon terminals in the outer lobula, its axon projects through the inner chiasm into the medulla where it branches and its cell body is located in a cortex of cell bodies adjacent to the medulla (Fig. S1)
To establish unequivocally that TmAs synapse with the LGMDs we used the ultrastructural evidence of synaptic contact provided by serial block-face-scanning electron microscopy (SBEM)[30,31]

Summary

Introduction

Of responses, a feature of the input organization of the LGMD 1 has been shown to be important, that of laterally spreading inhibition[18,22,23]. Synapses onto the LGMDs are cholinergic, activating calcium permeable nicotinic ACh receptors (nAChR) in the LGMD 1 and leading to its excitation[20,25,28]. These synaptic calcium signals reflect inputs which add together in a strongly sub-linear way in dendrites of the LGMD 116,17,24,29. No systematic anatomical evidence exists for universal lateral connections between the neurons providing input to the LGMDs. In single sections, synaptic interconnections between inputs onto one of the LGMDs have been reported but from single sections it is not clear what the three dimensional arrangement of synapses is, or how common these are[18,25]. We use a neural network simulating input to an LGMD to test the functional consequences of our findings

Methods

Results

Conclusion