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      Photoreceptor Processing Speed and Input Resistance Changes during Light Adaptation Correlate with Spectral Class in the Bumblebee, Bombus impatiens

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      PLoS ONE
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          Abstract

          Colour vision depends on comparison of signals from photoreceptors with different spectral sensitivities. However, response properties of photoreceptor cells may differ in ways other than spectral tuning. In insects, for example, broadband photoreceptors, with a major sensitivity peak in the green region of the spectrum (>500 nm), drive fast visual processes, which are largely blind to chromatic signals from more narrowly-tuned photoreceptors with peak sensitivities in the blue and UV regions of the spectrum. In addition, electrophysiological properties of the photoreceptor membrane may result in differences in response dynamics of photoreceptors of similar spectral class between species, and different spectral classes within a species. We used intracellular electrophysiological techniques to investigate response dynamics of the three spectral classes of photoreceptor underlying trichromatic colour vision in the bumblebee, Bombus impatiens, and we compare these with previously published data from a related species, Bombus terrestris. In both species, we found significantly faster responses in green, compared with blue- or UV-sensitive photoreceptors, although all 3 photoreceptor types are slower in B. impatiens than in B. terrestris. Integration times for light-adapted B. impatiens photoreceptors (estimated from impulse response half-width) were 11.3±1.6 ms for green photoreceptors compared with 18.6±4.4 ms and 15.6±4.4 for blue and UV, respectively. We also measured photoreceptor input resistance in dark- and light-adapted conditions. All photoreceptors showed a decrease in input resistance during light adaptation, but this decrease was considerably larger (declining to about 22% of the dark value) in green photoreceptors, compared to blue and UV (41% and 49%, respectively). Our results suggest that the conductances associated with light adaptation are largest in green photoreceptors, contributing to their greater temporal processing speed. We suggest that the faster temporal processing of green photoreceptors is related to their role in driving fast achromatic visual processes.

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          Most cited references49

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          A sensorimotor account of vision and visual consciousness.

          Many current neurophysiological, psychophysical, and psychological approaches to vision rest on the idea that when we see, the brain produces an internal representation of the world. The activation of this internal representation is assumed to give rise to the experience of seeing. The problem with this kind of approach is that it leaves unexplained how the existence of such a detailed internal representation might produce visual consciousness. An alternative proposal is made here. We propose that seeing is a way of acting. It is a particular way of exploring the environment. Activity in internal representations does not generate the experience of seeing. The outside world serves as its own, external, representation. The experience of seeing occurs when the organism masters what we call the governing laws of sensorimotor contingency. The advantage of this approach is that it provides a natural and principled way of accounting for visual consciousness, and for the differences in the perceived quality of sensory experience in the different sensory modalities. Several lines of empirical evidence are brought forward in support of the theory, in particular: evidence from experiments in sensorimotor adaptation, visual "filling in," visual stability despite eye movements, change blindness, sensory substitution, and color perception.
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            Motion and vision: why animals move their eyes.

            Nearly all animals with good vision have a repertoire of eye movements. The majority show a pattern of stable fixations with fast saccades that shift the direction of gaze. These movements may be made by the eyes themselves, or the head, or in some insects the whole body. The main reason for keeping gaze still during fixations is the need to avoid the blur that results from the long response time of the photoreceptors. Blur begins to degrade the image at a retinal velocity of about 1 receptor acceptance angle per response time. Some insects (e.g. hoverflies) stabilise their gaze much more rigidly than this rule implies, and it is suggested that the need to see the motion of small objects against a background imposes even more stringent conditions on image motion. A third reason for preventing rotational image motion is to prevent contamination of the translational flow-field, by which a moving animal can judge its heading and the distances of objects. Some animals do let their eyes rotate smoothly, and these include some heteropod molluscs, mantis shrimps and jumping spiders, all of which have narrow linear retinae which scan across the surroundings. Hymenopteran insects also rotate during orientation flights at speeds of 100-200 degrees s-1. This is just consistent with a blur-free image, as are the scanning speeds of the animals with linear retinae.
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              The metabolic cost of neural information.

              We derive experimentally based estimates of the energy used by neural mechanisms to code known quantities of information. Biophysical measurements from cells in the blowfly retina yield estimates of the ATP required to generate graded (analog) electrical signals that transmit known amounts of information. Energy consumption is several orders of magnitude greater than the thermodynamic minimum. It costs 10(4) ATP molecules to transmit a bit at a chemical synapse, and 10(6)-10(7) ATP for graded signals in an interneuron or a photoreceptor, or for spike coding. Therefore, in noise-limited signaling systems, a weak pathway of low capacity transmits information more economically, which promotes the distribution of information among multiple pathways.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                27 October 2011
                : 6
                : 10
                : e25989
                Affiliations
                [1]Biological and Experimental Psychology Group, School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
                Lund University, Sweden
                Author notes

                Conceived and designed the experiments: PS LC. Performed the experiments: PS. Analyzed the data: PS. Wrote the paper: PS LC.

                Article
                PONE-D-11-05251
                10.1371/journal.pone.0025989
                3203109
                22046251
                a29ba483-a7a2-4f58-ba69-a222dbedc1cd
                Skorupski, Chittka. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 22 March 2011
                : 15 September 2011
                Page count
                Pages: 8
                Categories
                Research Article
                Biology
                Computational Biology
                Computational Neuroscience
                Sensory Systems
                Ecology
                Ecophysiology
                Neuroscience
                Computational Neuroscience
                Sensory Systems
                Sensory Systems
                Visual System
                Zoology
                Entomology

                Uncategorized
                Uncategorized

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