Abstract
Specialized ommatidia harboring polarization-sensitive photoreceptors exist in the ‘dorsal rim area’ (DRA) of virtually all insects. Although downstream elements have been described both anatomically and physiologically throughout the optic lobes and the central brain of different species, little is known about their cellular and synaptic adaptations and how these shape their functional role in polarization vision. We have previously shown that in the DRA of Drosophila melanogaster, two distinct types of modality-specific ‘distal medulla’ cell types (Dm-DRA1 and Dm-DRA2) are post-synaptic to long visual fiber photoreceptors R7 and R8, respectively. Here we describe additional neuronal elements in the medulla neuropil that manifest modality-specific differences in the DRA region, including DRA-specific neuronal morphology, as well as differences in the structure of pre- or post-synaptic membranes. Furthermore, we show that certain cell types (medulla tangential cells and octopaminergic neuromodulatory cells) specifically avoid contacts with polarization-sensitive photoreceptors. Finally, while certain transmedullary cells are specifically absent from DRA medulla columns, other subtypes show specific wiring differences while still connecting the DRA to the lobula complex, as has previously been described in larger insects. This hints towards a complex circuit architecture with more than one pathway connecting polarization-sensitive DRA photoreceptors with the central brain.
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Abbreviations
- 24B10:
-
Monoclonal antibody against Chaoptin (photoreceptor marker)
- A:
-
Anterior
- AD:
-
Activation domain (split GAL4)
- AOTU:
-
Anterior optic tubercle
- B:
-
Blue
- BDSC:
-
Bloomington Drosophila Stock Center
- BRP:
-
Bruchpilot (marker of presynaptic active zones), as in brpD3 (short fragment)
- D:
-
Dorsal
- DBD:
-
DNA-binding domain (split GAL4)
- Dm:
-
Distal medulla (designation of cell type), as in Dm2, Dm4, Dm8, Dm9
- DRA:
-
Dorsal rim area
- DRA.R7:
-
R7 photoreceptor cell from DRA ommatidia
- DRA.R8:
-
R8 photoreceptor cell from DRA ommatidia
- DRep2:
-
Marker of putative post-synaptic membranes
- eq:
-
Equator of the eye
- FLP:
-
Flip recombinase (‘flippase’)
- G:
-
Green
- GAL4:
-
Transcription factor (binary expression system)
- GFP:
-
Green fluorescent protein
- GMR:
-
Glass multimeric reporter, as in longGMR
- GRASP:
-
GFP reconstitution across synaptic partners (technique)
- L:
-
Lateral
- La:
-
Lamina (neuropil)
- LexA:
-
Transcriptional activator recognizing LexAop binding sites
- Lo:
-
Lobula (neuropil)
- Lp:
-
Lobula plate (neuropil)
- M:
-
Medulla layer, as in M3 or M6
- mCD8:
-
GFP: Membrane-tagged GFP
- MCFO:
-
Multi-color Flp out (technique)
- Me:
-
Medulla (neuropil)
- mKate:
-
Red-fluorescent protein
- Mt:
-
Medulla tangential (cell type)
- NCad:
-
N-Cadherin (neuropil marker)
- PBS:
-
Phosphate buffered saline
- R:
-
Photoreceptor, as in R7 or R8
- Rh:
-
Rhodopsin, as in rh3
- Tdc:
-
Tyrosine decarboxylase
- TH:
-
Tyrosine hydroxylase
- Tm:
-
Transmedullary (cell type), as in Tm5a,b or Tm5c, Tm20
- Tom:
-
Tomato (red fluorescent protein)
- UAS:
-
Upstream activated sequences (recognized by GAL4)
- UV:
-
Ultraviolet
- VLP:
-
Ventrolateral protocerebrum
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Acknowledgements
The authors would like to thank Stephan Sigrist and Robin Hiesinger for sharing fly stocks and reagents, as well as two anonymous reviewers who made helpful suggestions on the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft (DFG) through Grants WE 5761/2-1 and SFB958 (Teilprojekt A23), through AFOSR grant FA9550-19-1-7005, through the Berlin Excellency Cluster NeuroCure, with support from the Fachbereich Biologie, Chemie & Pharmazie of the Freie Universität Berlin, as well as the Division of Neurobiology at Freie Universität Berlin (support of FU Berlin and the National Institute of Health to Robin Hiesinger).
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Sancer, G., Kind, E., Uhlhorn, J. et al. Cellular and synaptic adaptations of neural circuits processing skylight polarization in the fly. J Comp Physiol A 206, 233–246 (2020). https://doi.org/10.1007/s00359-019-01389-3
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DOI: https://doi.org/10.1007/s00359-019-01389-3