Binocular responsiveness of projection neurons of the praying mantis optic lobe in the frontal visual field

Abstract

Praying mantids are the only insects proven to have stereoscopic vision (stereopsis): the ability to perceive depth from the slightly shifted images seen by the two eyes. Recently, the first neurons likely to be involved in mantis stereopsis were described and a speculative neuronal circuit suggested. Here we further investigate classes of neurons in the lobula complex of the praying mantis brain and their tuning to stereoscopically-defined depth. We used sharp electrode recordings with tracer injections to identify visual projection neurons with input in the optic lobe and output in the central brain. In order to measure binocular response fields of the cells the animals watched a vertical bar stimulus in a 3D insect cinema during recordings. We describe the binocular tuning of 19 neurons projecting from the lobula complex and the medulla to central brain areas. The majority of neurons (12/19) were binocular and had receptive fields for both eyes that overlapped in the frontal region. Thus, these neurons could be involved in mantis stereopsis. We also find that neurons preferring different contrast polarity (bright vs dark) tend to be segregated in the mantis lobula complex, reminiscent of the segregation for small targets and widefield motion in mantids and other insects. Keywords Insect stereopsis • Praying mantis • 3D vision • Binocular vision • Depth perception Abbreviations ALO Anterior lobe of the lobula complex (ALO-V,D = ventral, dorsal subunits) DLO Dorsal lobe of the lobula complex INP Inferior neuropils LA Lamina LOX Lobula complex ME Medulla OL Optic lobe OLO Outer lobe of the lobula complex (OLO1, OLO2 = 1st, 2nd neuropil from distally) SLO Stalk lobe of the lobula complex VLNP Ventrolateral neuropils VMNP Ventromedial neuropils Electronic supplementary material The online version of this article (

Binocular Mirror-Symmetric Microsaccadic Sampling EnablesDrosophilaHyperacute 3D-Vision

“…Recordings from real neurons suggest that the depth estimation requires a change in the object’s visual distance, as shown for the praying mantis ( 37 ). If the object distance did not change, the suggested depth neurons would operate like many neurons along the motion detection pathway, responding most strongly to some preferred motion-direction yet showing less clear speed- or intensity-dependency.…”

“…An animal perceives motion when an object moves in its visual field and/or when itself or its eyes move (self-motion). For diurnal insects, praying mantis has been shown to estimate the distance to a moving object ( 37, 93 ). The distance between the left and right eye causes a depth ( z ) dependent delay between the corresponding left and right eye photoreceptor responses when their RFs collect light information from the same small visual area in space ( fig.…”

“…In the insect brain, the lobula complex neuropile pools visual information from ipsi- and contralateral eyes ( 35–37 ). This section describes the identification of a class of binocularly projecting lobula neurons: LC14 neurons in Drosophila .…”

“…Therefore, theoretically, this dynamic sampling can reliably feed the fly brain with 3D hyperacute information flow. In the centers interlinking the binocular inputs ( 34 ), such as the lobula complex ( 35–37 ) (fig. S57 to S60), the distance of an object crossing the corresponding left and right eye photoreceptor RFs could then be represented as distance in time ( Fig.…”

Visual circuits in arthropod brains

“…The optic lobe, especially the lobula complex, of these insects shows a number of highly specific organizational features not found in other insects. Rosner et al (2020) used sophisticated 3D virtual stimulation devices to analyze the binocular tuning of projection neurons of the medulla and lobula complex of these insects that are likely to participate in the stereoscopic network.…”