Integration of optic flow into the sky compass network in the brain of the desert locust

Abstract

Flexible orientation through any environment requires a sense of current relative heading that is updated based on self-motion. Global external cues originating from the sky or the earth's magnetic field and local cues provide a reference frame for the sense of direction. Locally, optic flow may inform about turning maneuvers, travel speed and covered distance. The central complex in the insect brain is associated with orientation behavior and largely acts as a navigation center. Visual information from global celestial cues and local landmarks are integrated in the central complex to form an internal representation of current heading. However, it is largely unclear which neurons integrate optic flow in the central-complex network. We recorded intracellularly from neurons in the locust central complex while presenting lateral grating patterns that simulated translational and rotational motion to identify these sites of integration. Certain types of central complex neurons were sensitive to visual self-motion independent of the type and direction of simulated motion. Columnar neurons innervating the noduli, paired central-complex substructures, were tuned to the direction of simulated horizontal turns. Modelling the connectivity of these neurons with a system of proposed compass neurons can account for rotation-direction specific shifts in the activity profile in the central complex corresponding to turn direction. Our model is similar but not identical to the mechanisms proposed for angular velocity integration in the navigation compass of the fly Drosophila.

The sky compass network in the brain of the desert locust

“…7e-e''). CL2 neurons show less robust tuning to polarized light than CL1 cells but, as suggested from two recordings of mirror symmetric CL2 cells, are sensitive to visual flow fields mimicking yaw rotation (Zittrell et al 2022). Like their counterparts in Drosophila, the PEN neurons (Green et al 2017;Turner-Evans et al 2017; Table 1), the CL2 neurons had opposite directional sensitivity: the neuron innervating the right nodulus was sensitive to simulated left turns, and the neuron innervating the left nodulus, to simulated right turns of the animal.…”

Parallel motion vision pathways in the brain of a tropical bee

“…While the pathway for transferring sky compass information from the eyes to the CX is well established across various insects (fruit fly: Hardcastle et al 2021 ; Warren et al 2019 ; monarch butterfly: Heinze and Reppert 2011 , 2012 ; Heinze et al 2013 ; locust: reviewed in el Jundi et al 2014 ; dung beetles: el Jundi et al 2015 ; Dacke and el Jundi 2018 ), much less is known about how optic flow information reaches this region. Although responses to wide field motion have been found in the CX of several insect species, these responses are either located in intrinsic neurons of the CX (columnar polarization sensitive neurons in locusts, Zittrell et al 2022 ; Rosner et al 2019 ), located in anatomically unidentified neurons (cockroach, Kathman et al 2014 ), or were generally weak, non direction- selective or state-dependent (locust, Rosner et al 2019 ; Zittrell et al 2022 ; flies, Weir et al 2014 ). In contrast, pronounced responses to optic flow, in particular to translational optic flow, were consistently identified in input neurons of the CX noduli (Bausenwein et al 1994 ; Stone et al 2017 ; Lu et al 2021 ).…”

Parallel motion vision pathways in the brain of a tropical bee

“…While the pathway for transferring sky compass information from the eyes to the CX is well established across various insects (fruit fly: Hardcastle et al (2021), Warren et al (2019); monarch butterfly: Heinze et al (2013), Heinze and Reppert (2011, 2012); locust: reviewed in el Jundi et al (2014); dung beetles: Dacke and el Jundi (2018), el Jundi et al (2015)), much less is known about how optic flow information reaches this region. Although responses to wide field motion have been found in the CX of several insect species, these responses are either located in intrinsic neurons of the CX (columnar polarization sensitive neurons in locusts, Rosner et al (2019), Zittrell et al (2022)), located in anatomically unidentified neurons (cockroach, Kathman et al (2014)), or were generally weak, non direction-selective or state-dependent (locust, Rosner et al (2019), Zittrell et al (2022); flies, Weir et al (2014)). In contrast, pronounced responses to optic flow, in particular to translational optic flow, were consistently identified in input neurons of the CX noduli (Bausenwein et al, 1994, Lu et al, 2021, Stone et al, 2017).…”