Integration of celestial compass cues in the central complex of the locust brain

Abstract

Many insects rely on celestial compass cues such as the polarization pattern of the sky for spatial orientation. In the desert locust, the central complex (CX) houses multiple sets of neurons, sensitive to the oscillation plane of polarized light and thus probably acts as an internal polarization compass. We investigated whether other sky compass cues like direct sunlight or the chromatic gradient of the sky might contribute to this compass. We recorded from polarization-sensitive CX neurons while an unpolarized green or ultraviolet light spot was moved around the head of the animal. All types of neuron that were sensitive to the plane of polarization (-vector) above the animal also responded to the unpolarized light spots in an azimuth-dependent way. The tuning to the unpolarized light spots was independent of wavelength, suggesting that the neurons encode solar azimuth based on direct sunlight and not on the sky chromatic gradient. Two cell types represented the natural 90 deg relationship between solar azimuth and zenithal -vector orientation, providing evidence to suggest that solar azimuth information supports the internal polarization compass. Most neurons showed advances in their tuning to the-vector and the unpolarized light spots dependent on rotation direction, consistent with anticipatory signaling. The amplitude of responses and its variability were dependent on the level of background firing, possibly indicating different internal states. The integration of polarization and solar azimuth information strongly suggests that besides the polarization pattern of the sky, direct sunlight might be an important cue for sky compass navigation in the locust.

GABA immunostaining in the central complex of dicondylian insects

“…The insect central complex has been suggested to serve roles in decision making and action selection (Ritzmann et al, 2012;Sun et al, 2017;Wolff & Strausfeld, 2016), control of locomotion (Martin, Guo, Mu, Harley, & Ritzmann, 2015;Strauss, 2002), spatial orientation and navigation (Heinze, 2017;Pfeiffer & Homberg, 2014;Turner-Evans & Jayaraman, 2016;Varga, Kathman, Martin, Guo, & Ritzmann, 2017), and, in Drosophila, promotion of sleep (Donlea et al, 2018;Liu et al, 2016). TL neurons provide sky compass information to the CBL in locusts, crickets, monarch butterflies, beetles, and bees (el Jundi et al, 2015;Heinze & Reppert, 2011;Homberg, Heinze, Pfeiffer, Kinoshita & el Jundi, 2011;Pegel, Pfeiffer, & Homberg, 2018;Sakura et al, 2008;Stone et al, 2017), and R neurons, heading direction relative to a bright target in fruit flies (Seelig & Jayaraman, 2013;Shiozaki & Kazama, 2017). Detailed analysis in Drosophila is beginning to dissociate different functional roles of R neuron subtypes regarding their visual receptive fields, involvement in spatial memory, signaling selfmotion turns, and mediating sleep drive (Liu et al, 2016;Ofstad et al, 2011;Shiozaki & Kazama, 2017).…”

Sun navigation requires compass neurons inDrosophila

“…The fly was surrounded by an array of LEDs on which we presented either a single 2.3° bright spot on a dark background or a 15°-wide dark vertical stripe on a bright background. Given previous studies on other species ( 4, 15, 16 ), we expect that flies react to our small bright spot as they would to the actual sun, and thus we call it a ‘sun stimulus’. Experiments were conducted in closed loop, such that the difference in stroke amplitude between the fly’s two wings determined the angular velocity of the stimulus ( 12 ).…”

“…Celestial cues such as sun position and polarized light are thought to be integrated in the central complex, a set of highly conserved unpaired neuropils in the central brain of arthropods ( 14 ). Central complex neurons in locusts ( 15 ), dung beetles ( 4 ), and monarch butterflies ( 16 ) respond to the angle of polarized light and the position of small bright objects mimicking the sun or moon. Extracellular recordings from the central complex in cockroaches revealed neurons that act as head-direction cells in the absence of visual cues or relative to a visual landmark ( 17 ).…”

The head direction circuit of two insect species

“…233 This difference reflected the utilisation of local inhibition in the case of the locust versus the global 234 inhibition in the fruit fly. Electrophysiologists have indeed reported this pronounced firing rate 235 variation in the locust [15,[47][48][49]. It will be interesting to see if the fruit fly neurons indeed show a 236 lower modulation as predicted by our model.…”