A visual pathway for skylight polarization processing inDrosophila

Abstract

SUMMARYMany 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.

A connectome of theDrosophilacentral complex reveals network motifs suitable for flexible navigation and context-dependent action selection

“…In other insects, some AOTU-projecting medullar columnar neurons (MeTus) are known to be tuned to polarized light e-vector orientations (Heinze, 2014), and such information is known to be present in the Drosophila medulla as well (Weir et al, 2016). A more recent study has confirmed that some classes of fly AOTU neurons, as well as their downstream partners, respond to polarized light stimuli much like in other insects (Hardcastle et al, 2020). We believe TuBu01 and TuBu06 neuron types are tuned to polarized light based both on their connectivity in the BU and on their arborization patterns in the AOTU ( Figure 6C, Dii, Figure 7D), but other types may also carry information about e-vector orientation.…”

“…A particularly strong contrast can be observed between the mapping of TuBu01 to ER4m, which is strictly one-to-one, preserving receptive fields (but not polarotopy (Hardcastle et al, 2020)), and TuBu06 to ER5, where multiple TuBu06 neurons contact a single ER5 neuron and single TuBu06 neurons project to multiple ER5 neurons ( Figure 7D,E, Figure 7-figure supplement 1B,C). This is noteworthy, as TuBu01 and TuBu06 receive input in the same region of the AOTU, but their downstream partners, ER4m and ER5 neurons, are known to have different functions: ER4m is tuned to polarized light (Hardcastle et al, 2020) and likely involved in visual orientation whereas ER5 neurons are involved in sleep (both will be discussed in more detail in later sections).…”

“…The full pathway comprises neurons that project from the photoreceptors to the medulla, the medulla to the AOTU, the AOTU to the BU, and the BU to the EB ( Figure 6A,B) (Homberg et al, 2003;Omoto et al, 2017;Sun et al, 2017). Across insects, some types of TuBu neurons (also called TuLAL1 neurons in some insects) are known to be tuned to polarized light e-vector orientations and visual features (el Jundi et al, 2014;Heinze and Reppert, 2011;Omoto et al, 2017;Pfeiffer et al, 2005;Sun et al, 2017), properties that they likely inherit from their inputs in the AOTU (Hardcastle et al, 2020;Omoto et al, 2017;Sun et al, 2017). In the fly, some TuBu neurons are known to respond strongly to bright stimuli on dark backgrounds (Omoto et al, 2017) or the orientation of polarized light e-vectors (Hardcastle et al, 2020), consistent with the idea that these neurons may be part of a sky compass pathway, as in other insects (el Jundi et al, 2018;Homberg et al, 2011).…”

“…These neurons pool medullary input from the visual field of one hemisphere and synapse onto a subset of TuBu neurons on the contralateral side. Note that at least one of these TuTuB neurons is known to be tuned to polarized light e-vector orientation (Hardcastle et al, 2020). The inter-hemispheric AOTU046 neurons receive input from multiple brain regions including both AOTUs, the BU (although they primarily send outputs there), the FB, and the ipsilateral (to their soma) IB and SPS (Figure 8Aii,Ci, Di, E).…”

“…Broadly, numerous experimental and computational studies suggest that the compass-like dynamics of the EPG population, which resemble those of a theorized network structure called a ring attractor (Kim et al, 2017b;Turner-Evans et al, 2020), are generated by the interaction of several neuron types (Cope et al, 2017;Fisher et al, 2019;Green et al, 2017;Kakaria and de Bivort, 2017;Kim et al, 2019;Turner-Evans et al, 2017;Turner-Evans et al, 2020). The neural compass relies on input from the anterior visual pathway to remain tethered to the fly's visual surroundings (Fisher et al, 2019;Hardcastle et al, 2020;Kim et al, 2019;Turner-Evans et al, 2020) and from mechanosensory ring neurons to tether to the direction of wind (Okubo et al, 2020). This representation of the fly's head direction is also updated by self-motion cues (Green et al, 2017;Turner-Evans et al, 2017) and persists even when the fly is standing still in darkness (Seelig and Jayaraman, 2015;Turner-Evans et al, 2020).…”