Spatial integration in polarization-sensitive interneurones of crickets: a survey of evidence, mechanisms and benefits

Abstract

SUMMARY Many insects exploit the polarization pattern of the sky for compass orientation in navigation or cruising-course control. Polarization-sensitive neurones (POL1-neurones) in the polarization vision pathway of the cricket visual system have wide visual fields of approximately 60° diameter, i.e. these neurones integrate information over a large area of the sky. This results from two different mechanisms. (i) Optical integration; polarization vision is mediated by a group of specialized ommatidia at the dorsal rim of the eye. These ommatidia lack screening pigment, contain a wide rhabdom and have poor lens optics. As a result, the angular sensitivity of the polarization-sensitive photoreceptors is very wide (median approximately 20°). (ii) Neural integration; each POL1-neurone receives input from a large number of dorsal rim photoreceptors with diverging optical axes. Spatial integration in POL1-neurones acts as a spatial low-pass filter. It improves the quality of the celestial polarization signal by filtering out cloud-induced local disturbances in the polarization pattern and increases sensitivity.

Polarimetry for Bionic Geolocation and Navigation Applications: A Review

“…After that, he found the same phenomenon in electrophysiological experiments on desert ants (Cataglyphis) [57]. In 2001, Labhart et al [24] conducted statistical experiments on POL-neurons of crickets and divided POL-neurons into three types that were approximately tuned to e-vector orientations of 10 • , 60 • , and 130 • , as shown in Figure 2e. The experimental results initially revealed the processing mechanism of polarization information in the optic lobe.…”

“…The radial scale indicates the number of POL-neurons found for any particular Φmax. There is a trimodal distribution of Φmax orientations consisting of three clearly separated peaks, indicating three types of POL-neurons tuned to e-vectors approximately 10°, 60°, and 130° [24]. [55].…”

“…Thus, it contains abundant pieces of directional and spatial information, and it provides a possibility for geolocation and navigation applications. Animals sense the skylight polarization pattern using a polarization-sensitive structure in compound eyes, and they figure out directions relying on the analysis of the polarization-sensitive nerve system [22][23][24], which enlightens human beings. The polarization of ubiquitous skylights has long been neglected because of the incapability of naked human eyes to perceive polarization directly.…”

Performance of polarization-sensitive neurons of the locust central complex at different degrees of polarization

“…Orientation to polarized light has been demonstrated for several insect species in the field (honey bees, Apis mellifera : von Frisch 1949 ; Evangelista et al 2014 ; desert ants, Cataglyphis fortis : Sommer and Wehner 2005 ; dung beetles, Scarabaeus satyrus : Dacke et al 2013 ) and in the laboratory (desert locusts, Schistocerca gregaria : Mappes and Homberg 2004 ; field crickets, Gryllus campestris : Brunner and Labhart 1987 ; monarch butterflies, Danaus plexippus : Reppert et al 2004 ). The neural pathways that mediate transmission of polarization information from the eye to the central brain have been studied particularly well in locusts (Homberg et al 2003 , 2011 ; Kinoshita et al 2007 ), crickets (Labhart 1988 ; Sakura et al 2007 ; Labhart et al 2001 ) and fruit flies (Hardcastle et al 2021 ) but also in other insects including monarch butterflies (Heinze and Reppert 2011 ) and dung beetles (el Jundi et al 2015 ). Specialized photoreceptors of a small, dorsal region of the compound eye, the dorsal rim area (DRA), are particularly sensitive to the oscillation angle of polarized light (Labhart and Meyer 1999 ).…”

Possible Role of Polarized Light Information in Spatial Recognition in the Cricket Gryllus bimaculatus

“…The specific region of the compound eye that detects the e-vector of the polarized skylight, called the dorsal rim area (DRA), has blue-sensitive photoreceptors that project their axons to the lamina or medulla in the optic lobe (Labhart et al, 1984;Blum and Labhart, 2000). In the medulla, a group of first-order polarization-sensitive neurons, called POL1 neurons, has been identified (Labhart, 1988;Labhart et al, 2001). At the higher center of the brain, another type of polarization-sensitive neurons, known as the tangential neurons in the central complex, potentially encode compass information (Sakura et al, 2007).…”