Non-Linear Neuronal Responses as an Emergent Property of Afferent Networks: A Case Study of the Locust Lobula Giant Movement Detector

In principle it appears advantageous for single neurons to perform non-linear operations. Indeed it has been reported that some neurons show signatures of such operations in their electrophysiological response. A particular case in point is the Lobula Giant Movement Detector (LGMD) neuron of the locust, which is reported to locally perform a functional multiplication. Given the wide ramifications of this suggestion with respect to our understanding of neuronal computations, it is essential that this interpretation of the LGMD as a local multiplication unit is thoroughly tested. Here we evaluate an alternative model that tests the hypothesis that the non-linear responses of the LGMD neuron emerge from the interactions of many neurons in the opto-motor processing structure of the locust. We show, by exposing our model to standard LGMD stimulation protocols, that the properties of the LGMD that were seen as a hallmark of local non-linear operations can be explained as emerging from the dynamics of the pre-synaptic network. Moreover, we demonstrate that these properties strongly depend on the details of the synaptic projections from the medulla to the LGMD. From these observations we deduce a number of testable predictions. To assess the real-time properties of our model we applied it to a high-speed robot. These robot results show that our model of the locust opto-motor system is able to reliably stabilize the movement trajectory of the robot and can robustly support collision avoidance. In addition, these behavioural experiments suggest that the emergent non-linear responses of the LGMD neuron enhance the system's collision detection acuity. We show how all reported properties of this neuron are consistently reproduced by this alternative model, and how they emerge from the overall opto-motor processing structure of the locust. Hence, our results propose an alternative view on neuronal computation that emphasizes the network properties as opposed to the local transformations that can be performed by single neurons.Author Summary: The tiny brains of insects of about 1mm3 smoothly control a flying platform while avoiding obstacles, regulating its distance to objects and search for objects of interest. This is largely achieved through a complex hierarchical processing of signals from the multitude of ommatidia in their eye to a set of highly specialized neurons that are optimized to respond to specific properties of the visual world. One of these neurons, the Lobula Giant Movement Detector (LGMD) of the locust, has been recently shown to perform a functional multiplication of its synaptic inputs. If true, that would make the LGMD neuron a unique and highly sophisticated neuron that raises questions about the non-linear operations other neurons in other neuronal systems would be able to perform. Hence it is crucial to understand its properties, its role in behaviour and to evaluate whether its responses can be explained in simpler terms. Our results emphasize the role of network architecture and distributed computation as opposed to local complex non-linear computation. We show that our model reliably reproduces the known properties of the LGMD and can be used to control a high-speed robot.