The sky compass network in the brain of the desert locust

Abstract

Many arthropods and vertebrates use celestial signals such as the position of the sun during the day or stars at night as compass cues for spatial orientation. The neural network underlying sky compass coding in the brain has been studied in great detail in the desert locust Schistocerca gregaria. These insects perform long-range migrations in Northern Africa and the Middle East following seasonal changes in rainfall. Highly specialized photoreceptors in a dorsal rim area of their compound eyes are sensitive to the polarization of the sky, generated by scattered sunlight. These signals are combined with direct information on the sun position in the optic lobe and anterior optic tubercle and converge from both eyes in a midline crossing brain structure, the central complex. Here, head direction coding is achieved by a compass-like arrangement of columns signaling solar azimuth through a 360° range of space by combining direct brightness cues from the sun with polarization cues matching the polarization pattern of the sky. Other directional cues derived from wind direction and internal self-rotation input are likely integrated. Signals are transmitted as coherent steering commands to descending neurons for directional control of locomotion and flight.

Behavioral responses of free flyingDrosophila melanogasterto shiny, reflecting surfaces

“…This knowledge is crucial for understanding how these signals are further processed by the brain, in order to inform behavioral responses. So far, the underlying pathways are understood only for the detection of celestial polarization, in some species (Weir, Henze et al 2016, Heinze 2017, Omoto, Keles et al 2017, Timaeus, Geid et al 2020, Hardcastle, Omoto et al 2021, Kind, Longden et al 2021, Sancer and Wernet 2021, Homberg, Hensgen et al 2022). The behavioral setup we present here now provides an efficient platform for the systematic dissection of the retinal substrate, as well as the underlying circuit elements in Drosophila melanogaster (Simpson 2009, Wernet, Huberman et al 2014).…”

Organization of descending neurons in the brain of the desert locust

“…The neuroarchitecture and functional role of the central complex has been studied in great detail in the desert locust (Homberg et al., 2023). The pattern of sky polarization and the azimuthal direction of direct sunlight are encoded in the locust central complex in a congruent, compass‐like manner (Zittrell et al., 2020).…”

“…The central complex, an interconnected group of neuropils in the insect brain, plays a key role in the control of navigational behavior and goal‐directed orientation (Strausfeld, 1999; Pfeiffer & Homberg, 2014; Varga et al., 2017; Fisher, 2022). As shown in several insect species, the central complex computes head orientation relative to external and internal cues (Heinze & Homberg, 2007); Zittrell et al., 2020; Honkanen et al., 2019); Fisher, 2022); Beetz et al., 2022), including sky compass signals (Heinze & Reppert, 2011); el Jundi et al., 2015); Pegel et al., 2018); Hardcastle et al., 2021); Homberg et al., 2023), information on wind direction (Okubo et al., 2020); Currier et al., 2020), internal turn‐related signals (Seelig & Jayaraman, 2015), as well as optic flow input (Stone et al., 2017) to generate goal‐directed steering commands.…”

“…The pattern of sky polarization and the azimuthal direction of direct sunlight are encoded in the locust central complex in a congruent, compass‐like manner (Zittrell et al., 2020). Central‐complex outputs target the lateral accessory lobes and several other brain areas (Heinze & Homberg, 2008 ; Hensgen et al., 2021; Homberg et al., 2023). Changes of neural activity in the central complex and lateral accessory lobe associated with flight motor activity (Homberg, 1994) indicate flight‐associated input and a role in flight motor control.…”

“…The pattern of sky polarization and the azimuthal direction of direct sunlight are encoded in the locust central complex in a congruent, compass-like manner (Zittrell et al, 2020). Central-complex outputs target the lateral accessory lobes and several other brain areas (Heinze & Homberg, 2008 ;Hensgen et al, 2021;Homberg et al, 2023).…”