Visual Reliability and Information Rate in the Retina of a Nocturnal Bee

Nocturnal animals relying on vision typically have eyes that are optically and morphologically adapted for both increased sensitivity and greater information capacity in dim light. Here, we investigate whether adaptations for increased sensitivity also are found in their photoreceptors by using closely related and fast-flying nocturnal and diurnal bees as model animals. The nocturnal bee Megalopta genalis is capable of foraging and homing by using visually discriminated landmarks at starlight intensities. Megalopta's near relative, Lasioglossum leucozonium, performs these tasks only in bright sunshine. By recording intracellular responses to Gaussian white-noise stimuli, we show that photoreceptors in Megalopta actually code less information at most light levels than those in Lasioglossum. However, as in several other nocturnal arthropods, Megalopta's photoreceptors possess a much greater gain of transduction, indicating that nocturnal photoreceptors trade information capacity for sensitivity. By sacrificing photoreceptor signal-to-noise ratio and information capacity in dim light for an increased gain and, thus, an increased sensitivity, this strategy can benefit nocturnal insects that use neural summation to improve visual reliability at night.

[1]  Karin Pirhofer-Walzl,et al.  Adaptations for vision in dim light: impulse responses and bumps in nocturnal spider photoreceptor cells (Cupienniussalei Keys) , 2007, Journal of Comparative Physiology A.

[2]  Eric J. Warrant,et al.  Neural organisation in the first optic ganglion of the nocturnal bee Megalopta genalis , 2004, Cell and Tissue Research.

[3]  P. Lillywhite,et al.  Single photon signals and transduction in an insect eye , 2004, Journal of comparative physiology.

[4]  M. Juusola,et al.  A method for determining photoreceptor signal-to-noise ratio in the time and frequency domains with a pseudorandom stimulus , 1994, Visual Neuroscience.

[5]  S B Laughlin,et al.  Variations in photoreceptor response dynamics across the fly retina. , 2001, Journal of neurophysiology.

[6]  C. Michener The Bees of the World , 2000 .

[7]  Eric J. Warrant,et al.  Light intensity limits foraging activity in nocturnal and crepuscular bees , 2006 .

[8]  Roger C. Hardie,et al.  Light Adaptation in Drosophila Photoreceptors , 2001, The Journal of general physiology.

[9]  C.E. Shannon,et al.  Communication in the Presence of Noise , 1949, Proceedings of the IRE.

[10]  E. Warrant Seeing better at night: life style, eye design and the optimum strategy of spatial and temporal summation , 1999, Vision Research.

[11]  M Järvilehto,et al.  Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors , 1994, The Journal of general physiology.

[12]  Eric J. Warrant,et al.  Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis , 2004, Cell and Tissue Research.

[13]  Mikko Vähäsöyrinki,et al.  The contribution of Shaker K+ channels to the information capacity of Drosophila photoreceptors , 2003, Nature.

[14]  J E Niven,et al.  Shaker K+-channels are predicted to reduce the metabolic cost of neural information in Drosophila photoreceptors , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  F. Prete Complex worlds from simpler nervous systems , 2004 .

[16]  Eric J. Warrant,et al.  Nocturnal Vision and Landmark Orientation in a Tropical Halictid Bee , 2004, Current Biology.

[17]  Eric J. Warrant,et al.  Neural Image Enhancement Allows Honeybees to See at Night , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[18]  M. Weckström,et al.  Spike-like potentials in the axons of nonspiking photoreceptors. , 1993, Journal of neurophysiology.

[19]  A. Dubs,et al.  The dynamics of phototransduction in insects , 1984, Journal of Comparative Physiology A.

[20]  R. Matthews,et al.  Ants. , 1898, Science.

[21]  Eric J. Warrant,et al.  A neural network to improve dim-light vision? Dendritic fields of first-order interneurons in the nocturnal bee Megalopta genalis , 2005, Cell and Tissue Research.

[22]  A. Dubs Non-Linearity and light adaptation in the fly photoreceptor , 1981, Journal of comparative physiology.

[23]  S. Laughlin,et al.  Transducer noise in a photoreceptor , 1979, Nature.

[24]  S. Laughlin,et al.  Fly Photoreceptors Demonstrate Energy-Information Trade-Offs in Neural Coding , 2007, PLoS biology.

[25]  Mikko Vähäsöyrinki,et al.  Robustness of Neural Coding in Drosophila Photoreceptors in the Absence of Slow Delayed Rectifier K+ Channels , 2006, The Journal of Neuroscience.

[26]  Barbara Blakeslee,et al.  The intracellular pupil mechanism and photoreceptor signal: noise ratios in the fly Lucilia cuprina , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[27]  S B Laughlin,et al.  Matched filtering by a photoreceptor membrane , 1996, Vision Research.

[28]  S. Laughlin,et al.  Temperature and the temporal resolving power of fly photoreceptors , 2000, Journal of Comparative Physiology A.

[29]  W. Wcislo,et al.  Flight performance in night-flying sweat bees suffers at low light levels , 2007, Journal of Experimental Biology.

[30]  S. B. Laughlin,et al.  Fast and slow photoreceptors — a comparative study of the functional diversity of coding and conductances in the Diptera , 1993, Journal of Comparative Physiology A.

[31]  J. H. Hateren,et al.  Theoretical predictions of spatiotemporal receptive fields of fly LMCs, and experimental validation , 1992, Journal of Comparative Physiology A.

[32]  S. Laughlin,et al.  The rate of information transfer at graded-potential synapses , 1996, Nature.

[33]  Michael F. Land,et al.  Optics and Vision in Invertebrates , 1981 .

[34]  M. Sanders Handbook of Sensory Physiology , 1975 .

[35]  Simon Laughlin,et al.  The sensitivity of receptors in the posterior median eye of the nocturnal spider,Dinopis , 1980, Journal of comparative physiology.

[36]  Kuno Kirschfeld,et al.  The Absolute Sensitivity of Lens and Compound Eyes , 1974, Zeitschrift fur Naturforschung. Section C, Biosciences.

[37]  Eric J. Warrant,et al.  Visual summation in night-flying sweat bees: A theoretical study , 2006, Vision Research.

[38]  A. S. French,et al.  Shaker K+ channels contribute early nonlinear amplification to the light response in Drosophila photoreceptors. , 2003, Journal of neurophysiology.

[39]  D. Ventura,et al.  Comparative study of temporal summation and response form in hymenopteran photoreceptors , 2004, Journal of Comparative Physiology A.

[40]  Matti Weckström,et al.  Large Functional Variability in Cockroach Photoreceptors: Optimization to Low Light Levels , 2006, The Journal of Neuroscience.

[41]  Eric Warrant,et al.  Vision in the dimmest habitats on Earth , 2004, Journal of Comparative Physiology A.

[42]  S B Laughlin,et al.  Intrinsic noise in locust photoreceptors. , 1982, The Journal of physiology.