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Locusts exhibit remarkable phenotypic plasticity changing their appearance and behavior from solitary to gregarious when population density increases. These changes include morphological differences in the size and shape of brain regions, but little is known about plasticity within individual neurons and alterations in behavior not directly related to aggregation or swarming. We investigated looming escape behavior and the properties of a well-studied collision-detection neuron in gregarious and solitarious animals of three closely related species, the desert locust (Schistocerca gregaria), the Central American locust (S. piceifrons) and the American bird grasshopper (S. americana). For this neuron, the lobula giant movement detector (LGMD), we examined dendritic morphology, membrane properties, gene expression, and looming responses. Gregarious animals reliably jumped in response to looming stimuli, but surprisingly solitarious desert locusts did not produce escape jumps. These solitarious animals also had smaller LGMD dendrites. This is the first study done on three different species of grasshoppers to observe the effects of phenotypic plasticity on the jump escape behavior, physiology and transcriptomics of these animals. Unexpectedly, there were little differences in these properties between the two phases except for behavior. For the three species, gregarious animals jumped more than solitarious animals, but no significant differences were found between the two phases of animals in the electrophysiological and transcriptomics studies of the LGMD. Our results suggest that phase change impacts mainly the motor system and that the physiological properties of motor neurons need to be characterized to understand fully the variation in jump escape behavior across phases. 

Neurons receive information through their synaptic inputs, but the functional significance of how those inputs are mapped on to a cell’s dendrites remains unclear. We studied this question in a grasshopper visual neuron that tracks approaching objects and triggers escape behavior before an impending collision. In response to black approaching objects, the neuron receives OFF excitatory inputs that form a retinotopic map of the visual field onto compartmentalized, distal dendrites. Subsequent processing of these OFF inputs by active membrane conductances allows the neuron to discriminate the spatial coherence of such stimuli. In contrast, we show that ON excitatory synaptic inputs activated by white approaching objects map in a random manner onto a more proximal dendritic field of the same neuron. The lack of retinotopic synaptic arrangement results in the neuron’s inability to discriminate the coherence of white approaching stimuli. Yet, the neuron retains the ability to discriminate stimulus coherence for checkered stimuli of mixed ON/OFF polarity. The coarser mapping and processing of ON stimuli thus has a minimal impact, while reducing the total energetic cost of the circuit. Further, we show that these differences in ON/OFF neuronal processing are behaviorally relevant, being tightly correlated with the animal’s escape behavior to light and dark stimuli of variable coherence. Our results show that the synaptic mapping of excitatory inputs affects the fine stimulus discrimination ability of single neurons and document the resulting functional impact on behavior.