Abstract
Dragonflies are highly skilled and successful aerial predators that are even capable of selectively attending to one target within a swarm. Detection and tracking of prey is likely to be driven by small target motion detector (STMD) neurons identified from several insect groups. Prior work has shown that dragonfly STMD responses are facilitated by targets moving on a continuous path, enhancing the response gain at the present and predicted future location of targets. In this study, we combined detailed morphological data with computational modeling to test whether a combination of dendritic morphology and nonlinear properties of NMDA receptors could explain these observations. We developed a hybrid computational model of neurons within the dragonfly optic lobe, which integrates numerical and morphological components. The model was able to generate potent facilitation for targets moving on continuous trajectories, including a localized spotlight of maximal sensitivity close to the last seen target location, as also measured during in vivo recordings. The model did not, however, include a mechanism capable of producing a traveling or spreading wave of facilitation. Our data support a strong role for the high dendritic density seen in the dragonfly neuron in enhancing non-linear facilitation. An alternative model based on the morphology of an unrelated type of motion processing neuron from a dipteran fly required more than three times higher synaptic gain in order to elicit similar levels of facilitation, despite having only 20% fewer synapses. Our data support a potential role for NMDA receptors in target tracking and also demonstrate the feasibility of combining biologically plausible dendritic computations with more abstract computational models for basic processing as used in earlier studies.
Highlights
Imagine a dragonfly hungry for breakfast, flying out over a small lake in the morning and searching for small prey to catch
We further developed this computational approach to investigate the possible role for N-methyl-D-aspartate receptor (NMDA) receptors in the facilitation of dragonfly small target motion detector (STMD) neurons, as introduced in our previous work (Shoemaker, 2011; Bekkouche et al, 2017)
We have reported here the analysis of NMDA-receptor-mediated response facilitation using an elaborated version of a model for which we previously reported the modeling framework (Bekkouche et al, 2017)
Summary
Imagine a dragonfly hungry for breakfast, flying out over a small lake in the morning and searching for small prey to catch. Complex excitatory and inhibitory interactions between both visual fields are mediated by heterolateral and centrifugal STMD neurons such as the identified cell CSTMD1 This neuron type has been identified in both dipteran flies and dragonflies (Nordström et al, 2006; Geurten et al, 2007), and has its inputs in the midbrain, with extensive arborizations in the contralateral lobula. We focus on the facilitation of responses to stimuli moving along long trajectories in the dragonfly BSTMD1 neuron, believed to play a key role in the dragonfly visual selective attention mechanism (Dunbier et al, 2012) This anatomical data was challenging and time consuming to acquire and is the first BSTMD1 morphology data with sufficiently high detail to be reconstructed in 3D and used for computational modeling. Despite varying the synaptic gain, we were unable to recruit such strong facilitation using an alternative model based on the anatomy of a fly wide-field motion neuron, suggesting that this property depends on the unique morphology of BSTMD1
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