The neuronal basis of insect stereopsis

Abstract

A puzzle for neuroscience -and robotics -is how insects achieve surprisingly 11 complex behaviours with such tiny brains 1,2 . One example is depth perception via 12 binocular stereopsis in the praying mantis, a predatory insect. Praying mantids use 13 stereopsis, the computation of distances from disparities between the two retinas, to 14 trigger a raptorial strike of their forelegs 3,4 when prey is within reach. The neuronal basis 15 of this ability is entirely unknown. From behavioural evidence, one view is that the mantis 16 brain must measure retinal disparity locally across a range of distances and 17 eccentricities 4-7 , very like disparity-tuned neurons in vertebrate visual cortex 8 . Sceptics 18 argue that this "retinal disparity hypothesis" implies far too many specialised neurons 19 for such a tiny brain 9 . Here we show the first evidence that individual neurons in the 20 praying mantis brain are indeed tuned to specific disparities and eccentricities, and thus 21 locations in 3D-space. This disparity information is transmitted to the central brain by 22 95 information to the contralateral optic lobe, but also receiving information from the contralateral 96 eye via other COcom-neurons, and in this way generating its binocularity (see below). 97Four of the binocular COcom-neurons showed evident binocular interactions in the 98 central parts of the response fields (at 15-100mm distance and 20 o eccentricity; Fig. 2d,f,g,j). 99Behavioural experiments 6 have shown that mantis stereopsis operates for prey capture over this 100 region of 3D-space. Three neurons had well-localised excitatory peaks ( Fig. 2d,f,g) for a 101 preferred 3D location. These were well modelled by combining binocular excitation at the 102 preferred location with inhibition in peripheral regions (Extended Data Fig. 4 a,b,c). In the 103 fourth neuron the central region was void of excitation, because of inhibition by input from the 104 contralateral eye in the centre of the visual field ( Fig. 2 j,k). In vertebrates such cells are known 105 as "tuned-inhibitory neurons", in contrast to "tuned-excitatory neurons" whose receptive fields 106 have a similar structure in both eyes 22 . The neuron from Fig. 2a,b,c,d also showed disparity 107 tuning to the spiralling disc stimulus (Wilcoxon rank-sum test p=0.0043, Fig. 2e). 108The morphology of two additional, disparity-sensitive neuron types suggests that they 109 convey information centrifugally (soma in central brain -Fig. 3a,c; beaded terminal neurites in 110 optic lobe -Extended Data Fig. 5) from the central brain to the LOX (TAcen-neurons) and the 111 medulla (TMEcen-neurons). All 5 TAcen-neurons tested with bright bars were clearly disparity 112 tuned (Fig. 3b, Extended Data Figs. 6). They have broad excitatory receptive fields with peak 113 response for far distances or even diverging lines of sight. Thus, TAcen-neurons are suited to 114 provide information about the distant, bright visual background in front of which dark prey-115 targets are detected by other classes of neuron...

Motion-in-depth perception and prey capture in the praying mantisSphodromantis lineola

“…An earlier model suggested that a complex of LGMD-DCMD-type neurons could also implement a simple form of stereopsis (Kral and Prete, 2004), which might then mean that the same set of neurons would detect both looming and stereoscopic stimuli. However, more recent work has instead implicated several neuronal types in the lobula complex in the computation of stereoscopic disparity in the mantises Hierodula membranacea and Rhombodera megaera (Rosner et al, 2019). In fact, the lobula complex in mantises appears to have a species-specific neuropil called the 'stalk lobe' that has been speculated to be involved in stereopsis (Rosner et al, 2017).…”

Mathematical study of neural feedback roles in small target motion detection

“…Insects selectively responded to salient visual stimuli via a close-loop in the brain (Paulk et al, 2014), which guided behavioral choices made by these insects. The feedback connection was discovered in the binocular stereopsis of praying mantis (Rosner et al, 2019), which calculated the distances from disparities between the two retinal images via feedback to trigger a raptorial strike of their forelegs when prey is within reach. In recent years, feedback mechanism has been proven to effectively improve model performance in many studies, including medical image segmentation (Soker, 2016) and object recognition (Wang and Huang, 2015).…”