Neural circuits underlying colour vision and visual memory in Drosophila melanogaster

Focusing at the fly visual system I am addressing the identity and
function of neurons accomplishing two fundamental processing steps
required for survival of most animals: neurons of peripheral
circuits underlying colour vision as well neurons of higher order
circuits underlying visual memory. Colour vision is commonly
assumed to rely on photoreceptors tuned to narrow spectral ranges.
In the ommatidium of Drosophila, the four types of so-called inner
photoreceptors express different narrow-band opsins. In contrast,
the outer photoreceptors have a broadband spectral sensitivity and
are thought to exclusively mediate achromatic vision. Using
computational models and behavioural experiments, I here
demonstrate that the broadband outer photoreceptors contribute to
colour vision in Drosophila. A model of opponent processing that
includes the opsin of the outer photoreceptors scores the best fit
to wavelength discrimination behaviour of flies. To experimentally
uncover the contribution of individual photoreceptor types, I used
blind flies with disrupted phototransduction (norpA-) and rescued
norpA function in genetically targeted photoreceptors and receptor
combinations. Surprisingly, dichromatic flies with only broadband
photoreceptors and one additional receptor type can discriminate
different colours, indicating the existence of a specific output
comparison of outer and inner photoreceptors. Furthermore, blocking
interneurons postsynaptic to the outer photoreceptors specifically
impairs colour but not intensity discrimination. These findings
show that outer receptors with a complex and broad spectral
sensitivity do contribute to colour vision and reveal that
chromatic and achromatic circuits in the fly share common
photoreceptors. Higher brain areas integrate sensory input from
different modalities including vision and associate these neural
representations with good or bad experiences. It is unclear,
however, how distinct sensory memories are processed in the
Drosophila brain. Furthermore, the neural circuit underlying
colour/intensity memory in Drosophila remained so far unknown. In
order to address these questions, I established appetitive and
aversive visual learning assays for Drosophila. These allow
contrasting appetitive and aversive visual memories using
neurogenetic methods for circuit analysis. Furthermore, the visual
assays are similar to the widely used olfactory learning assays and
share reinforcing stimuli (sugar reward and electric shock
punishment), conditioning regimes and methods for memory
assessment. Thus, a direct comparison of the cellular requirements
for visual and olfactory memories becomes feasible. I found that
the same subsets of dopamine neurons innervating the mushroom body
are necessary and sufficient for formation of both sensory
memories. Furthermore, expression of D1-like Dopamine Receptor
(DopR) in the mushroom body is sufficient to restore the memory
defect of a DopR null mutant (dumb-). These findings and the
requirement of the mushroom body for visual memory in the used
assay suggest that the mushroom body is a site of convergence,
where representations of different sensory modalities may undergo
associative modulation.