A neural model for insect steering applied to olfaction and path integration

Abstract

Many animal behaviours require orientation and steering with respect to the environment. For insects, a key brain area involved in spatial orientation and navigation is the central complex. Activity in this neural circuit has been shown to track the insects current heading relative to its environment, and has also been proposed to be the substrate of path integration. However, it remains unclear how the output of the central complex is integrated into motor commands. Central complex output neurons project to the lateral accessory lobes (LAL), from which descending neurons project to thoracic motor centres. Here, we present a computational model of a simple neural network that has been described anatomically and physiologically in the LALs of male silkworm moths, in the context of odour-mediated steering. We present and analyze two versions of this network, both implemented in the Nengo framework, one rate-based and one based on spiking neurons. The modelled network consists of an inhibitory local interneuron and a bistable descending neuron ( flip-flop), which both receive input in the LAL. The flip-flop neuron projects onto neck motor neurons to induce steering. We show that this simple computational model not only replicates the basic parameters of male silkworm moth behaviour in a simulated odour plume, but can also take input from a computational model of path integration in the central complex and use it to steer back to a point of origin. Furthermore, we find that increasing the level of detail within the model improves the realism of the models behaviour. Our results suggest that descending neurons originating in the lateral accessory lobes, such as flip-flop neurons, are sufficient to mediate multiple steering behaviours. This study is therefore a first step to close the gap between orientation circuits in the central complex and downstream motor centres. Author summaryTargeted movements and steering within an environment are essential for many behaviours. In insects, the brains center for spatial orientation and navigation is the central complex, which processes information about the configuration of the local environment as well as global orientation cues such as the Sun position. Neural networks in the central complex also compute the insects heading direction, and are thought to be involved in generating steering commands. However, it is unclear how these steering commands are transmitted to downstream motor centers. Output neurons from the central complex project to the lateral accessory lobes, a neuropil which also gives rise to descending pre-motor neurons that are involved in steering in the silkworm moth Bombyx mori. In this study, we provide a computational model of a pre-motor neural network in the lateral accessory lobes. We show that this network can steer an agent towards the source of a simulated odor plume, but that it can also steer efficiently when getting input from an anatomically constrained network model of the central complex. This model is therefore a first step to close the gap between the central complex and thoracic motor circuits.