The neuronal basis of insect stereopsis

Abstract

A puzzle for neuroscience - and robotics - is how insects achieve surprisingly complex behaviours with such tiny brains1,2. One example is depth perception via binocular stereopsis in the praying mantis, a predatory insect. Praying mantids use stereopsis, the computation of distances from disparities between the two retinas, to trigger a raptorial strike of their forelegs3,4 when prey is within reach. The neuronal basis of this ability is entirely unknown. From behavioural evidence, one view is that the mantis brain must measure retinal disparity locally across a range of distances and eccentricities4-7, very like disparity-tuned neurons in vertebrate visual cortex8. Sceptics argue that this \"retinal disparity hypothesis\" implies far too many specialised neurons for such a tiny brain9. Here we show the first evidence that individual neurons in the praying mantis brain are indeed tuned to specific disparities and eccentricities, and thus locations in 3D-space. This disparity information is transmitted to the central brain by neurons connecting peripheral visual areas in both hemispheres, as well as by a unilateral neuron type. Like disparity-tuned cortical cells in vertebrates, the responses of these mantis neurons are consistent with linear summation of binocular inputs followed by an output nonlinearity10. Additionally, centrifugal neurons project disparity information back from the central brain to early visual areas, possibly for gain modulation or 3D spatial attention. Thus, our study not only proves the retinal disparity hypothesis for insects, it reveals feedback connections hitherto undiscovered in any animal species.