Convergent escape behavior from distinct visual processing of impending collision in fish and grasshoppers

Abstract

In animal species ranging from invertebrate to mammals, visually guided escape behaviors 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 behaviors. 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 collision detecting neurons in grasshoppers were sensitive to acceleration whereas the triggering of escape behaviors was less so. In contrast, neurons in goldfish identified indirectly through the characteristic features of the escape behaviors they trigger, showed little sensitivity to acceleration. This closely mirrored a broader lack of sensitivity to acceleration of the goldfish escape behavior. Thus, although the sensory coding of simulated colliding stimuli with non-zero acceleration likely differs in grasshoppers and goldfish, the triggering of escape behaviors converges towards similar characteristics. Approaching stimuli with non-zero acceleration may help refine our understanding of neural computations underlying escape behaviors in a broad range of animal species. Key pointsO_LIA companion manuscript showed that two mathematical models of collision-detecting neurons in grasshoppers and goldfish make distinct predictions for their responses to simulated objects approaching on a collision course with non-zero acceleration. C_LIO_LITesting 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. C_LIO_LIBoth the escape behaviors of grasshopper and goldfish were insensitive to acceleration suggesting a further transformation downstream in grasshopper motor circuits that matches the computation observed in the goldfish Mauthner cell. C_LIO_LIThus, in spite of different sensory processing in the two species, escape behaviors converge towards similar solutions. C_LIO_LIThe 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. C_LI