A visual pathway for skylight polarization processing in Drosophila

Abstract

Many insects use patterns of polarized light in the sky to orient and navigate. Here we functionally characterize neural circuitry in the fruit fly, Drosophila melanogaster, that conveys polarized light signals from the eye to the central complex, a brain region essential for the fly's sense of direction. Neurons tuned to the angle of polarization of ultraviolet light are found throughout the anterior visual pathway, connecting the optic lobes with the central complex via the anterior optic tubercle and bulb, in a homologous organization to the 'sky compass' pathways described in other insects. We detail how a consistent, map-like organization of neural tunings in the peripheral visual system is transformed into a reduced representation suited to flexible processing in the central brain. This study identifies computational motifs of the transformation, enabling mechanistic comparisons of multisensory integration and central processing for navigation in the brains of insects.

Organization and neural connections of the lateral complex in the brain of the desert locust

“…The LX consists of two distinct areas, the bulbs (BUs) and the LAL (Ito et al, 2014). The BUs are clusters of microglomerular complexes that relay spatial visual information from the lower unit of the anterior optic tubercle to the CBL (Hardcastle et al, 2021; Held et al, 2016; Mota et al, 2016; Omoto et al, 2017; Seelig & Jayaraman, 2013, 2015; Shiozaki & Kazama, 2017; Träger et al, 2008). The LAL mediates various other sensory input, such as optic flow information toward the noduli (Stone et al, 2017), wind direction signals to the central body (Currier et al, 2020; Okubo et al, 2020), and self‐generated proprioceptive information to the central body (Homberg, 1994; Hulse et al, 2020).…”

Flight-induced compass representation in the monarch butterfly heading network

“…Within the E-PG network, heading is represented by a single activity bump that changes its position when the insect changes its heading direction 13,16 . The activity bump in E-PG cells results from the integration of visual signals and mechanosensory information 14,[17][18][19] , as well as idiothetic, self-motion signals 13,20,21 .…”

Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila

“…In the DRA, the inner photoreceptors express the same UV rhodopsin (Rh3; Fortini and Rubin 1991, 1990) and detect perpendicular angles of polarized UV light (Weir et al 2016). In contrast to the rest of the medulla, R7-DRA and R8-DRA project to the same medulla layer (M6; Chin et al 2014; Pollack and Hofbauer 1991; Fischbach and Dittrich 1989), where their targets include polarization-specific cell types (Sancer et al 2019, 2020; Hardcastle et al 2021). Across insects, a ‘compass pathway’ connects the DRA to the central brain via the anterior optic tubercle (AOTU; Homberg 2015; Hardcastle et al 2021; Pfeiffer and Kinoshita 2012).…”

“…In contrast to the rest of the medulla, R7-DRA and R8-DRA project to the same medulla layer (M6; Chin et al 2014; Pollack and Hofbauer 1991; Fischbach and Dittrich 1989), where their targets include polarization-specific cell types (Sancer et al 2019, 2020; Hardcastle et al 2021). Across insects, a ‘compass pathway’ connects the DRA to the central brain via the anterior optic tubercle (AOTU; Homberg 2015; Hardcastle et al 2021; Pfeiffer and Kinoshita 2012). Anatomical and functional data from Drosophila suggests that the central medulla is also connected to the compass pathway (Omoto et al 2017; Hardcastle et al 2021; Otsuna et al 2014), potentially forming parallel pathways for processing different celestial cues (Timaeus et al 2020; Tai et al 2021).…”

“…Across insects, a ‘compass pathway’ connects the DRA to the central brain via the anterior optic tubercle (AOTU; Homberg 2015; Hardcastle et al 2021; Pfeiffer and Kinoshita 2012). Anatomical and functional data from Drosophila suggests that the central medulla is also connected to the compass pathway (Omoto et al 2017; Hardcastle et al 2021; Otsuna et al 2014), potentially forming parallel pathways for processing different celestial cues (Timaeus et al 2020; Tai et al 2021).…”