Wide-Field Motion Integration in Fly VS Cells: Insights from an Inverse Approach

Fly lobula plate tangential cells are known to perform wide-field motion integration. It is assumed that the shape of these neurons, and in particular the shape of the subclass of VS cells, is responsible for this type of computation. We employed an inverse approach to investigate the morphology-function relationship underlying wide-field motion integration in VS cells. In the inverse approach detailed, model neurons are optimized to perform a predefined computation: here, wide-field motion integration. We embedded the model neurons to be optimized in a biologically plausible model of fly motion detection to provide realistic inputs, and subsequently optimized model neuron with and without active conductances (gNa, gK, gK(Na)) along their dendrites to perform this computation. We found that both passive and active optimized model neurons perform well as wide-field motion integrators. In addition, all optimized morphologies share the same blueprint as real VS cells. In addition, we also found a recurring blueprint for the distribution of gK and gNa in the active models. Moreover, we demonstrate how this morphology and distribution of conductances contribute to wide-field motion integration. As such, by using the inverse approach we can predict the still unknown distribution of gK and gNa and their role in motion integration in VS cells.Author Summary: It is well established that neuronal morphology influences the computation performed by a single neuron. However, it remains largely unknown how these computations emerge from the interaction between dendritic morphology, the distribution of ion-channels and synaptic inputs. To investigate this neuronal morphology-function relationship we employ an inverse approach in which detailed model neurons are optimized to perform a predefined computation. In this work, we set to investigate how dendritic morphology contributes to wide-field motion integration in fly lobula plate tangential cells (LPTCs), cells of which the morphology is assumed to be linked to their function as wide-field motion integrators. The resulting optimized models perform well and share crucial features of LPTC morphology. By analysis of the optimized models, we revealed a match between morphological structures and physiological mechanisms required to perform wide-field motion integration, i.e., we explicitly show the morphology-function relationship in LPTC neurons. Moreover, the optimized distribution of ionic conductances gives rise to predictions about the distribution and role of these conductances in the real neurons. Finally, our findings provide an explanation of dendritic morphologies in terms of the computation they should perform.