Multiple Redundant Medulla Projection Neurons Mediate Color Vision in Drosophila

Abstract

The receptor mechanism for color vision has been extensively studied. In contrast, the circuit(s) that transform(s) photoreceptor signals into color percepts to guide behavior remain(s) poorly characterized. Using intersectional genetics to inactivate identified subsets of neurons, we have uncovered the first-order interneurons that are functionally required for hue discrimination in Drosophila. We developed a novel aversive operant conditioning assay for intensity-independent color discrimination (true color vision) in Drosophila. Single flying flies are magnetically tethered in an arena surrounded by blue and green LEDs (light-emitting diodes). The flies’ optomotor response is used to determine the blue-green isoluminant intensity. Flies are then conditioned to discriminate between equiluminant blue or green stimuli. Wild-type flies are successfully trained in this paradigm when conditioned to avoid either blue or green. Functional color entrainment requires the function of the narrow-spectrum photoreceptors R8 and/or R7, and is within a limited range, intensity independent, suggesting that it is mediated by a color vision system. The medulla projection neurons, Tm5a/b/c and Tm20, receive direct inputs from R7 or R8 photoreceptors and indirect input from the broad-spectrum photoreceptors R1–R6 via the lamina neuron L3. Genetically inactivating these four classes of medulla projection neurons abolished color learning. However, inactivation of subsets of these neurons is insufficient to block color learning, suggesting that true color vision is mediated by multiple redundant pathways. We hypothesize that flies represent color along multiple axes at the first synapse in the fly visual system. The apparent redundancy in learned color discrimination sharply contrasts with innate ultraviolet (UV) spectral preference, which is dominated by a single pathway from the amacrine neuron Dm8 to the Tm5c projection neurons.

Keywords::

• color discrimination
• medulla projection neurons
• neural substrate
• visual behavior

ACKNOWLEDGMENTS

We thank Martin Heisenberg for suggestions on behavioral assays, Michael Reiser and Mark Frye for help with the magnetic tethering system, Craig Montell and Benjamin White for fly lines, and Claude Desplan and Nina Vogt for communicating results prior to publication. This work was supported by the Intramural Research Programs of the NIH, Eunice Kennedy Shriver National Institute of Child Health and Human Development (grant Z01-HD008776 to C.-H.L) and Center for Information Technology (R.P. and T.P.), and the intramural funds of the National Institute of Biomedical Imaging and Bioengineering (P.D.S.).

Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.