Comprehensive map of visual projection neurons for processing ultraviolet information in the Drosophila brain

Abstract

The brain perceives visual information and controls behavior depending on its underlying neural circuits. How UV information is represented and processed in the brain remains poorly understood. In Drosophila melanogaster, UV light is detected by the R7 photoreceptor that projects exclusively into the medulla layer 6 (M 6). Herein, we imaged 28,768 single neurons and identified 238 visual projection neurons linking M 6 to the central brain. Based on morphology and connectivity, these visual projection neurons were systematically classified into 94 cell types belonging to 12 families. Three tracts connected M 6 in each optic lobe to the central brain: One dorsal tract linking to the ipsilateral lateral anterior optic tubercle (L-AOTU) and two medial tracts linking to the ipsilateral ventral medial protocerebrum (VMP) and the contralateral VMP. The M 6 information was primarily represented in the L-AOTU. Each L-AOTU consisted of four columns that each contained three glomeruli. Each L-AOTU glomerulus received inputs from M 6 subdomains and gave outputs to a glomerulus within the ellipsoid body dendritic region, suggesting specific processing of spatial information through the dorsal pathway. Furthermore, the middle columns of the L-AOTUs of both hemispheres were connected via the intertubercle tract, suggesting information integration between the two eyes. In contrast, an ascending neuron linked each VMP to all glomeruli in the bulb and the L-AOTU, bilaterally, suggesting general processing of information through the ventral pathway. Altogether, these diverse morphologies of the visual projection neurons suggested multi-dimensional processing of UV information through parallel and bilateral circuits in the Drosophila brain.

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

“…Central R7 and R7-DRA cells are strongly connected to different classes of MeTu cells, which form long axons terminating in spatially segregated areas of the small unit of the AOTU (Figure 10E). Previous studies proposed that different kinds of visual information may be processed by distinct parallel pathways leading towards the central brain via the AOTU (Otsuna, Shinomiya, and Ito 2014;Omoto et al 2017;Timaeus et al 2020;Tai, Chin, and Chiang 2021). Our reconstructions support this hypothesis, showing different target regions for these 2 putative MeTu types, and functional measurements confirm that the target area of MeTu-DRA cells shows polarization-sensitive responses (Hardcastle et al 2021).…”

“…Nearly 10% of the synapses made by the central seed column R7 and R8 photoreceptors were with cells projecting directly to the central brain. Of these, the strongest targets were the MeTu cells, which resemble Tm cells, but instead of sending axons to the lobula, projected to the anterior optic tubercule (AOTU) via the anterior optic tract (Fischbach and Lyly-Hunerberg 1983;Otsuna, Shinomiya, and Ito 2014;Otsuna and Ito 2006;Omoto et al 2017;Timaeus et al 2020;Tai, Chin, and Chiang 2021;Figure 5A). Our reconstructions confirmed that MeTu cells were indeed synaptic targets of R7 (Timaeus et al 2020), and that their photoreceptor input was exclusively from R7 (Figure 5Aiv).…”

“…We found 7 such neurons, and reconstructed the complete morphology of one. Their dendrites overlapped and covered ~20-30 columns (Figure 5Aii), while the axons all targeted the lateral tip of the AOTU (Timaeus et al 2020;Omoto et al 2017;Tai, Chin, and Chiang 2021;Figure 5Ai).…”

“…Drosophila suggests that the central medulla is also connected to the compass pathway (Omoto et al 2017;Hardcastle et al 2021;Otsuna, Shinomiya, and Ito 2014), potentially forming parallel pathways for processing different celestial cues (Timaeus et al 2020;Tai, Chin, and Chiang 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).…”