Interactions between Dpr11 and DIP-γ control selection of amacrine neurons in Drosophila color vision circuits

Abstract

Drosophila R7 UV photoreceptors (PRs) are divided into yellow (y) and pale (p) subtypes. yR7 PRs express the Dpr11 cell surface protein and are presynaptic to Dm8 amacrine neurons (yDm8) that express Dpr11’s binding partner DIP-γ, while pR7 PRs synapse onto DIP-γ-negative pDm8. Dpr11 and DIP-γ expression patterns define ‘yellow’ and ‘pale’ color vision circuits. We examined Dm8 neurons in these circuits by electron microscopic reconstruction and expansion microscopy. DIP-γ and dpr11 mutations affect the morphologies of yDm8 distal (‘home column’) dendrites. yDm8 neurons are generated in excess during development and compete for presynaptic yR7 PRs, and interactions between Dpr11 and DIP-γ are required for yDm8 survival. These interactions also allow yDm8 neurons to select yR7 PRs as their appropriate home column partners. yDm8 and pDm8 neurons do not normally compete for survival signals or R7 partners, but can be forced to do so by manipulation of R7 subtype fate.

Color vision in insects: insights from Drosophila

“…Anatomical data show that Tm5a, which is found exclusively in y columns, receives input from R7y but not R7p, and that Tm5b receives predominately input from R7p (Fig. 4c) (Karuppudurai et al 2014;Menon et al 2019). In contrast, Tm5c appears to pool p and y inputs (Fig.…”

“…Analysis of the expression of the surface molecules of the Dpr and DIP family suggests that different flavors of Dm8 exist that likely correspond with p and y subtypes. Dpr11 is selectively expressed in R7y that contact a subpopulation of Dm8 that in turn express the Dpr11 interaction partner DIP-γ; absence of these interaction partners characterize R7p and another subpopulation of Dm8 (Carrillo et al 2015;Tan et al 2015;Menon et al 2019).…”

“…Dm8 is postsynaptic to R7, has multi-columnar organization, and expresses Ort. Individual Dm8 cells pool 'UV input' from 12 to 16 R7 photoreceptors of neighboring ommatidia and conveys it to all Tm5 subtypes, as well as unknown neurons (Gao et al 2008;Karuppudurai et al 2014;Menon et al 2019). Blocking synaptic output of glutamatergic Dm8 results in reduced preference for UV, whereas flies with restored Ort receptor function in exclusively Dm8 (cell specific Dm8 rescue in ort mutant flies) exhibit intact spectral preference behavior (Gao et al 2008).…”

R7 photoreceptor axon targeting depends on the relative levels oflost and foundexpression in R7 and its synaptic partners

“…The populations of cholinergic and glutamatergic neurons include other synaptic targets of Loaf, making the matching hypothesis still a possibility. To test the involvement of the cholinergic neurons Tm5a and Tm5b (Davis et al, 2020), which are postsynaptic to R7 (Gao et al, 2008, Menon et al, 2019, we used GMR9D03-GAL4, which is expressed in a subset of these cells ( Figure 5 -figure supplement 1A, B). Expressing Loaf with this driver in a loaf mutant background again produced significant R7 mistargeting ( Figure 5A, H), consistent with the hypothesis that R7 matches its Loaf levels to Tm5a/b.…”

“…However, it is not known whether R7 relies on Dm8 for targeting or survival information; the Dm8 dendrites that remain in the absence of R7 cells still project to the M6 layer (Courgeon and Desplan, 2019). Many synapses between R7 and Dm8 also include the projection neurons Tm5a (yR7) or Tm5b (pR7) as a second postsynaptic element (Gao et al, 2008, Takemura et al, 2015, Menon et al, 2019. In addition, Dm9 interneurons are both pre-and postsynaptic to R7 and mediate center-surround inhibition, similarly to horizontal cells in the mammalian retina (Takemura et al, 2013, Takemura et al, 2015, Heath et al, 2020.…”