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AbstractIn animal species ranging from invertebrate to mammals, visually guided escape behaviours have been studied using looming stimuli, the two‐dimensional expanding projection on a screen of an object approaching on a collision course at constant speed. The peak firing rate or membrane potential of neurons responding to looming stimuli often tracks a fixed threshold angular size of the approaching stimulus that contributes to the triggering of escape behaviours. To study whether this result holds more generally, we designed stimuli that simulate acceleration or deceleration over the course of object approach on a collision course. Under these conditions, we found that the angular threshold conveyed by collision detecting neurons in grasshoppers was sensitive to acceleration whereas the triggering of escape behaviours was less so. In contrast, neurons in goldfish identified through the characteristic features of the escape behaviours they trigger, showed little sensitivity to acceleration. This closely mirrored a broader lack of sensitivity to acceleration of the goldfish escape behaviour. Thus, although the sensory coding of simulated colliding stimuli with non‐zero acceleration probably differs in grasshoppers and goldfish, the triggering of escape behaviours converges towards similar characteristics. Approaching stimuli with non‐zero acceleration may help refine our understanding of neural computations underlying escape behaviours in a broad range of animal species.image Key pointsA companion manuscript showed that two mathematical models of collision‐detecting neurons in grasshoppers and goldfish make distinct predictions for the timing of their responses to simulated objects approaching on a collision course with non‐zero acceleration.Testing these experimental predictions showed that grasshopper neurons are sensitive to acceleration while goldfish neurons are not, in agreement with the distinct models proposed previously in these species using constant velocity approaches.Grasshopper and goldfish escape behaviours occurred after the stimulus reached a fixed angular size insensitive to acceleration, suggesting further downstream processing in grasshopper motor circuits to match what was observed in goldfish.Thus, in spite of different sensory processing in the two species, escape behaviours converge towards similar solutions.The use of object acceleration during approach on a collision course may help better understand the neural computations implemented for collision avoidance in a broad range of species. 

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. 

The central nervous system (CNS) is specialised in processing information originating from a variety of internal and external sources. Its basic information processing units are nerve cells or neu- rons. Within the CNS, these elementary building blocks are densely interconnected in hierarchical and parallel pathways. Information originating from sensory neurons in contact with the body periphery is gradually transformed along these pathways to generate specific actions through signals relayed by motor neurons to peripheral organs. Information processing in the CNS exhibits an astonishing degree of diversity when con- sidering the morphology of its neurons, their connectivity patterns, their electrical and their biochemical signalling properties. Thus, the infor- mation processing capabilities of animal brains are quite distinct from those of existing man-made machines, being characterised by their resilience to noise, their capacity to rapidly adapt, learn and generalise, as well as their ability to participate in complex social behaviours.