Hue selectivity from recurrent circuitry in Drosophila.

In the perception of color, wavelengths of light reflected off objects are transformed into the derived quantities of brightness, saturation and hue. Neurons responding selectively to hue have been reported in primate cortex, but it is unknown how their narrow tuning in color space is produced by upstream circuit mechanisms. We report the discovery of neurons in the Drosophila optic lobe with hue-selective properties, which enables circuit-level analysis of color processing. From our analysis of an electron microscopy volume of a whole Drosophila brain, we construct a connectomics-constrained circuit model that accounts for this hue selectivity. Our model predicts that recurrent connections in the circuit are critical for generating hue selectivity. Experiments using genetic manipulations to perturb recurrence in adult flies confirm this prediction. Our findings reveal a circuit basis for hue selectivity in color vision.

Hue selectivity from recurrent circuitry in Drosophila.

A universal principle of sensory perception is the progressive transformation of sensory information from broad non-specific signals to stimulus-selective signals that form the basis of perception. To perceive color, our brains must transform the wavelengths of light reflected off objects into the derived quantities of brightness, saturation and hue. Neurons responding selectively to hue have been reported in primate cortex, but it is unknown how their narrow tuning in color space is produced by upstream circuit mechanisms. To enable circuit level analysis of color perception, we here report the discovery of neurons in the Drosophila optic lobe with hue selective properties. Using the connectivity graph of the fly brain, we construct a connectomics-constrained circuit model that accounts for this hue selectivity. Unexpectedly, our model predicts that recurrent connections in the circuit are critical for hue selectivity. Experiments using genetic manipulations to perturb recurrence in adult flies confirms this prediction. Our findings reveal the circuit basis for hue selectivity in color vision.

Exploiting colour space geometry for visual stimulus design across animals.

Colour vision represents a vital aspect of perception that ultimately enables a wide variety of species to thrive in the natural world. However, unified methods for constructing chromatic visual stimuli in a laboratory setting are lacking. Here, we present stimulus design methods and an accompanying programming package to efficiently probe the colour space of any species in which the photoreceptor spectral sensitivities are known. Our hardware-agnostic approach incorporates photoreceptor models within the framework of the principle of univariance. This enables experimenters to identify the most effective way to combine multiple light sources to create desired distributions of light, and thus easily construct relevant stimuli for mapping the colour space of an organism. We include methodology to handle uncertainty of photoreceptor spectral sensitivity as well as to optimally reconstruct hyperspectral images given recent hardware advances. Our methods support broad applications in colour vision science and provide a framework for uniform stimulus designs across experimental systems. This article is part of the theme issue 'Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods'.

Flexible filtering by neural inputs supports motion computation across states and stimuli.

Sensory systems flexibly adapt their processing properties across a wide range of environmental and behavioral conditions. Such variable processing complicates attempts to extract a mechanistic understanding of sensory computations. This is evident in the highly constrained, canonical Drosophila motion detection circuit, where the core computation underlying direction selectivity is still debated despite extensive studies. Here we measured the filtering properties of neural inputs to the OFF motion-detecting T5 cell in Drosophila. We report state- and stimulus-dependent changes in the shape of these signals, which become more biphasic under specific conditions. Summing these inputs within the framework of a connectomic-constrained model of the circuit demonstrates that these shapes are sufficient to explain T5 responses to various motion stimuli. Thus, our stimulus- and state-dependent measurements reconcile motion computation with the anatomy of the circuit. These findings provide a clear example of how a basic circuit supports flexible sensory computation.

Circuit Mechanisms Underlying Chromatic Encoding in Drosophila Photoreceptors.

Spectral information is commonly processed in the brain through generation of antagonistic responses to different wavelengths. In many species, these color opponent signals arise as early as photoreceptor terminals. Here, we measure the spectral tuning of photoreceptors in Drosophila. In addition to a previously described pathway comparing wavelengths at each point in space, we find a horizontal-cell-mediated pathway similar to that found in mammals. This pathway enables additional spectral comparisons through lateral inhibition, expanding the range of chromatic encoding in the fly. Together, these two pathways enable efficient decorrelation and dimensionality reduction of photoreceptor signals while retaining maximal chromatic information. A biologically constrained model accounts for our findings and predicts a spatio-chromatic receptive field for fly photoreceptor outputs, with a color opponent center and broadband surround. This dual mechanism combines motifs of both an insect-specific visual circuit and an evolutionarily convergent circuit architecture, endowing flies with the ability to extract chromatic information at distinct spatial resolutions.