Abstract
True colour vision requires comparing the responses of different spectral classes of photoreceptors. In insects, there is a wealth of data available on the physiology of photoreceptors and on colour-dependent behaviour, but less is known about the neural mechanisms that link the two. The available information in bees indicates a diversity of colour opponent neurons in the visual optic ganglia that significantly exceeds that known in humans and other primates. Here, we present a simple mathematical model for colour processing in the optic lobes of bees to explore how this diversity might arise. We found that the model can reproduce the physiological spectral tuning curves of the 22 neurons that have been described so far. Moreover, the distribution of the presynaptic weights in the model suggests that colour-coding neurons are likely to be wired up to the receptor inputs randomly. The perceptual distances in our random synaptic weight model are in agreement with behavioural observations. Our results support the idea that the insect nervous system might adopt partially random wiring of neurons for colour processing.
Highlights
Bees are extensively studied for their colour vision
The spatial antagonism between the centre and surround in the receptive fields of retinal ganglion cells and a set of additional modulatory processes ensure that there are two classes of cone opponent processes, with predictable inputs from the three spectral receptor types, that form the foundation of colour opponency and colour perception as measurable in psychophysical experiments[15,22,23,24,25,26,27]
We compiled the available information on neuron morphology[38,51], electrophysiology[28,29,30,38] and immunohistochemistry[38,52,53,54] relevant to colour sensitive neurons in bees (Apis mellifera and Bombus impatiens) and deduced a simple model of circuitry that is in line with our current knowledge (Fig. 1)
Summary
Behavioural[1,2,3] and electrophysiological[4,5,6] work has established that the vision of most species of bees is trichromatic, receiving input from three spectral types of photoreceptors whose sensitivity peaks in the UV (for honeybees, λmax ≈ 344 nm), blue (for honeybees, λmax ≈ 436 nm) and green (for honeybees, λmax ≈ 544 nm) parts of the spectrum These wavelength positions are close to the theoretical optimum for coding flower colours[7]. Theoretical work assumed deterministic wiring from receptors to colour sensitive neurons, and indicated that two spectrally antagonistic neuron types might explain colour discrimination in bees[35,36] (perhaps inspired by the colour opponency mechanisms in humans). Advances in machine learning have shown that such randomness can lead to efficient representations in neural networks[49,50]
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