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Mechanisms of Achromatic Vision in Invertebrates and Vertebrates: A Comparative Study

Published online by Cambridge University Press:  10 January 2013

Alexander M. Chernorizov  and
Evgenii N. Sokolov
Alexander M. Chernorizov*
Affiliation:
Lomonosov Moscow State University (Russia)
Evgenii N. Sokolov
Affiliation:
Lomonosov Moscow State University (Russia)
*
Correspondence concerning this article should be addressed to Dr. Alexander M. Chernorizov. Department of Psychophysiology. Faculty of Psychology. Lomonosov Moscow State University. Mokhovaya St., 11/5. 125009 Moscow. (Russia). E-mail: [email protected]
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Abstract

Intracellular recording in the retina of the snail, Helix pomatia L., reveals the existence of two types of cell responsive to diffuse flashes of achromatic or monochromatic light: B-type cells, which respond with sustained depolarization that is sometimes accompanied by spikes, and D-type cells, which respond with sustained hyperpolarization. The peak of spectral sensitivity for both B- and D-cells falls in the 450-500 nm range and coincides with range of maximal sensitivity for the rhodopsin family of photopigments. Within a proposed two-channel model of snail achromatic vision, responses of the B- and D-cells are represented by a two-dimensional ‘excitation vector’. The length of the ‘excitation vector’ is approximately constant, and its direction correlates with light intensity. The vector model of light encoding in the snail is discussed in relation to models of achromatic vision in vertebrates (fish, frog, monkey, and humans) based on psychophysical, behavioral and neurophysiological data. Intracellular data in the snail taken together with data from vertebrate animals support the hypothesis that a 2-dimensional model of brightness and darkness encoding utilizes a universal mechanism of ‘vector encoding’ for light intensity in neuronal vision networks.

El registro intracelular en la retina del caracol, Heliz pomatia, L., muestra la existencia de dos tipos de células que reaccionan a destellos difusos de luz acromática o monocromática: las células tipo B responden con una depolarización constante con picos de actividad ocasionales; y las células tipo D responden con una hiperpolarización constante. El pico de sensibilidad espectral de las células B y C se centra en un rango de entre 450-500 nm y coincide con los rangos de máxima sensibilidad de las rodopsinas, de la familia de los fotopigmentos. Desde el modelo de dos-canales de visión acromática del caracol, las respuestas a las células B y D están representadas por un vector de excitación de dos-canales. La extensión de este vector de excitación es más o menos constante, y su dirección correlaciona con la intensidad de la luz. El procesamiento de la luz de los caracoles se discute en términos del modelo del vector en relación con modelos de visión acromática en vertebrados (peces, ranas, monos, y humanos) basados en datos psicofisiológicos, conductuales y neurofisiológicos. Tomados en conjunto, los datos intracelulares del caracol y los de animales vertebrados se sostiene la hipótesis de que el modelo de 2-dimensiones para el procesamiento del brillo y la oscuridad se basa en un mecanismo universal de codificación vectorial para la intensidad de la luz en las redes neuronales de visión.

Keywords

achromatic visionretinamolluskbrightness and darkness neuronsvector encodingvisión acromáticaretinamoluscobrillo y oscuridadneuronascodificación vectorial
Type
Research Article
Information
The Spanish Journal of Psychology , Volume 13 , Issue 1 , May 2010 , pp. 18 - 29
Copyright
Copyright © Cambridge University Press 2010

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Footnotes

†Professor Y.N. Sokolov passed away on May 14, 2008.

References

Chalupa, L.M., & Gunhan, E. (2004). Development of ON and OFF retinal pathways and retinogeniculate projections. Progress in retinal and eye research, 23(1), 31–51.CrossRefGoogle Scholar
Chernorizov, A.M. (1999). Neyronnye mekhanizmy tsvetovogo zreniya [Neural mechanisms of color vision]. Doctoral Thesis. Moscow: Lomonosov Moscow State University Press.Google Scholar
Chernorizov, A.M., Shekhter, E.D., Arakelov, G.G., & Zimachev, M.M. (1994). The Vision of the Snail: The Spectral Sensitivity of the Dark-Adapted Eye. Neurocsience & Behavioral Physiology, 24 (1), 59–62.CrossRefGoogle ScholarPubMed
Chernorizov, A.M., & Sokolov, E.N. (2001). Vektornoe kodirovanie tsveta v sloe bipolyarnykh kletok setchatki karpa [Vector encoding of color in bipolar cells of carp retina]. Vestnik MGU. Seriya 14. Psikhologiya, 1, 12–35.Google Scholar
Clarke, R.J., & Ikeda, H. (1985). Luminance and darkness detectors in the olivary and posterior pretectal nuclei and their relationship to the pupillary light reflex in the rat. I. Studies with steady luminance levels. Experimental Brain Research, 57 (2), 224–232.CrossRefGoogle Scholar
De Valois, R.L., & De Valois, K.K. (1975). Neural coding of color. In De Valois, R. & De Valois, K. (Eds.), Handbook of perception. Vol. 5. Seeing (pp. 117–166). N.Y.- San Francisco -London: Springer-Verlag.Google Scholar
Eakin, R.M., & Brandenburger, J.L. (1967). Differentiation in the eye of a pulmonate snail Helix aspersa. Journal of Ultrastructure Research, 18 (4), 391–421.CrossRefGoogle ScholarPubMed
Evtikhin, D.V., Polyanskiy, V.B., Alymkulov, D.E., & Sokolov, E.N. (2008). Coding of Luminance and Color Differences on Neurons in the Rabbit's Visual System. The Spanish Journal of Psychology, 11 (2), 349–362.CrossRefGoogle ScholarPubMed
Gomez, M. del P., & Nasi, E. (1998). Membrane current induced by protein kinase C activators in rhabdomeric photoreceptors: implications for visual excitation. Journal of Neuroscience, 18 (14), 5253–5263.CrossRefGoogle Scholar
Gomez, M. del P., & Nasi, E. (2000). Light transduction in invertebrate hyperpolarizing photoreceptors: possible involvement of a Go-regulated guanylate cyclase. Journal of Neuroscience, 20 (14), 5254–5263.CrossRefGoogle ScholarPubMed
Hartline, H.K. (1940). The nerve messages in the fibers of the visual pathway. Journal of Optical Society of America, 30, 239–247.CrossRefGoogle Scholar
Heggelund, P. (1992). A bidimensional theory of achromatic color vision. Vision Research, 32, 2107–2119.CrossRefGoogle ScholarPubMed
Izmailova, T.V., Sokolov, E.N., Izmailov, Ch.A., & Livshits, G.Ya. (1988). Obshchaya sfericheskaya model' razlicheniya tsvetovykh signalov [A universal spherical model for differentiation of color signals]. Voprosy psikhologii, 1, 137–149.Google Scholar
Izmailov, Ch.A., Sokolov, E.N., & Chernorizov, A.M. (1989). Psikhofiziologiya tsvetovogo zreniya [Psychophysiology of Color Vision]. Moskva: Izdatel'stvo MGU.Google Scholar
Izmailov, Ch.A., Isaichev, S.A., & Shekhter, E.D. (1998). Dvukhkanal'naya model' razlicheniya signalov v sensornykh sistemakh [Two-channel model for differentiation of signals in sensory systems]. Vestnik MGU. Seriya 14. Psikhologiya, 3, 29–40.Google Scholar
Izmailov, Ch.A., & Sokolov, E.N. (1991). Spherical model of color and brightness discrimination. Psychological Science, 2, 249–259.CrossRefGoogle Scholar
Izmailov, Ch.A., Zimachev, M.M., Sokolov, E.N., & Chernorizov, A.M. (2006). Dvukhkanal'naya model' akhromaticheskogo zreniya lyagushki [Two-channel model of achromatic vision in frog]. Zhurnal Sensornye systemy, 20 (1), 1–11.Google Scholar
Judd, D. B., & Wyszecki, G. (1975). Color in business, science and industry (3rd ed.). New York / London / Sydney / Toronto: Wiley J. & Sons.Google Scholar
Jung, R. (1973). Visual perception and neurophysiology. In Jung, R. & Autrum, H. (Eds.), Handbook of Sensory Physiology. V. 7/3. Central Processing of Visual Information. Part A (pp. 1–153). Heidelberg, Berlin: Springer-Verlag.Google Scholar
Kolb, H., Fernandez, E., & Nelson, R. (2008). The Organization of the Retina and Visual System. Part II. Anatomy and Physiology of the Retina. In WEBVISION. Retrieved December 20, 2008, from http:/retina.umh.es/webvision_Google Scholar
Kulaichev, A.P. (2002). Komp'yuternaya electrofiziologiya [Computer electrophysiology]. Moskva: Izdatel'stvo MGU.Google Scholar
Kusunoki, M, Moutoussis, K, & Zeki, S. (2006). Effect of background colors on the tuning of color-selective cells in monkey area V4. Journal of Neurophysiology, 95(5), 3047–3059.CrossRefGoogle ScholarPubMed
Latanov, A.V., Polyanskiy, V.B., & Sokolov, E.N. (1991). Chetyrekh-mernoe tsvetovoe prostranstvo obez'yany [Four-dimensional color space for monkey]. Zhurnal Vysshei Nervnoi Deyatel'nosti Im I.P. Pavlova, 41 (4), 636–646.Google Scholar
Latanov, A.V., Leonova, A.Yu., Evtikhin, D.V., & Sokolov, E.N. (1997). Sravnitel'naya neirobiologiya tsvetovogo zreniya cheloveka i zhivotnykh [Comparative neurobiology of color vision in human and animals]. Zhurnal Vysshei Nervnoi Deyatel'nosti Im I.P. Pavlova, 47 (2), 308–320.Google Scholar
Leonova, A.Yu., Latanov, A.V., Polianskii, V.B., & Sokolov, E.N. (1994). Pertseptivnoe tsvetovoe prostranstvo karpa [Perceptual color space of carp]. Zhurnal Vysshei Nervnoi Deyatel'nosti Im I.P. Pavlova, 44 (6), 1059–1069.Google Scholar
Leonov, Yu. P., & Sokolov, E.N. (2006). Spherical color space with Riemann geometry. ECVP- 2006. 29th European Conference on Visual Perception, 35, Supplement, 1.Google Scholar
Leonov, Yu. P., & Sokolov, E.N. (2008). The Representation of Colors in Spherical Space. Journal Color research and application, 33(2), 113–124.CrossRefGoogle Scholar
Magnussen, Sv., Bjorklund, R.A., & Kruger, Ju. (2008). The perception of flicker: Theoretical note on the relation between brightness and darkness enhancement. Scandinavian Journal of Psychology, 20 (1), 257–258.CrossRefGoogle Scholar
Manookin, M.B., Beaudoin, D.L., Ernst, Z.R., Flagel, L.J., & Demb, J.B. (2008). Disinhibition Combines with Excitation to Extend the Operating Range of the OFF Visual Pathway in Daylight. Journal of Neuroscience, April 16, 28 (16), 4136–4150.CrossRefGoogle ScholarPubMed
McReynolds, J.S., & Gorman, A.L.F. (1970). Photoreceptor potentials of opposite polarity in the eye of the scallop, Pecten irradians. Journal of General Physiology, 56, 376–391.CrossRefGoogle ScholarPubMed
Musio, C. (2001). Patch-clamping solitary visual cells to understand the cellular mechanisms of invertebrate phototransduction. In Musio, C. (Ed.), Vision: Approach of Biophysics and Neuroscience (pp. 145–164). Singapore: World Scientific Publishing Co. Pte. Ltd.CrossRefGoogle Scholar
Nasi, E. (1991a). Electrophysiological properties of isolated photoreceptors from the eye of Lima scabra. Journal of General Physiology, 97 (1), 17–34.CrossRefGoogle ScholarPubMed
Nasi, E. (1991b). Whole-cell clamp of dissociated photoreceptors from the eye of Lima scabra. Journal of General Physiology, 97 (1), 35–54.CrossRefGoogle ScholarPubMed
Nasi, E. (1991c). Two light-dependent conductances in Lima rhabdomeric photoreceptors. Journal of General Physiology, 97 (1), 55–72.CrossRefGoogle ScholarPubMed
Nordsieck, R. (2008). The Roman snail (Helix pomatia L.): Senses and Sense Organs. In The Living World of Mollusks. Retrieved November 27, 2008, from http://www.weichtiere.at/Mollusks/Schnecken/weinberg.html.2008Google Scholar
Pang, Ji-Jie, Gao, F., & Wu, S.M. (2003). Light-Evoked Excitatory and Inhibitory Synaptic Inputs to ON and OFF α Ganglion Cells in the Mouse Retina. Journal of Neuroscience, 23 (14), 6063–6073.CrossRefGoogle Scholar
Poggio, G.F., Baker, F.H., Lamarre, Y., & Sanseverino, E.R. (1969). Afferent inhibition at input to visual cortex of the cat. Journal of Neurophysiology, 32 (6), 892–915.CrossRefGoogle ScholarPubMed
Polyanskii, V.B., Evtikhin, D.V., & Sokolov, E.N. (2005). Vychislenie tsvetovykh i yarkostnykh razlichiy neyronami zritel'noy kory krolika [Computation of color and brightness differences by neurons in the rabbit visual cortex]. Zhurnal Vysshei Nervnoi Deyatel'nosti Im I.P. Pavlova, 55 (1), 60–70.Google Scholar
Polyanskii, V.B., Evtikhin, D.V., Sokolov, E.N., & Alymkulov, D.E. (2006). Vychislenie tsvetovykh i yarkostnykh razlichiy neyronami lateral'nogo kolenchatogo tela krolika [Computation of color and brightness differences by neurons in the rabbit lateral geniculate nucleus]. Zhurnal Vysshei Nervnoi Deyatel'nosti Im I.P. Pavlova, 56 (1): 74–84.Google Scholar
Polyanskii, V.B., Alymkulov, D.E., Evtikhin, D.V., & Sokolov, E.N. (2008). Assessment of Brightness and Color Differences by Neurons in the Superior Colliculus of the Rabbit. Neuroscience and Behavioral Physiology, 38 (9), 971–983.CrossRefGoogle ScholarPubMed
Shekhter, E.D., Zimachev, M.M., & Arakelov, G.G. (1992). Zrenie vinogradnoy ulitki. Morfologiya i summarnaya elektricheskaya aktivnost' setchatki [Vision in grape snail. Morphology and summary electrical activity of retina]. Zhurnal Vysshei Nervnoi Deyatel'nosti Im I.P. Pavlova, 42 (5), 986–992.Google Scholar
Shekhter, E.D., & Grechenko, T.N. (2009). Dva tipa fotoretsoptorof v akhromaticheskoy zritel'noy sisteme vinogradnoy ulitki [Two types of photoreceptors in achromatic visual system of Helix Pomatia]. Eksperimental'naya psikhologiya, 2 (2), 5–15.Google Scholar
Sokolov, E.N. (2000). Perception and the conditioning reflex: vector encoding. International Journal of Psychophysiology, 35, 197–217.CrossRefGoogle ScholarPubMed
Sokolov, E.N. (2003). Vospriyatie i uslovnyy refleks. Novyy vzglyad [Perception and Conditioning Reflex. New Approach]. Moskva: UMK Psikhologiya.Google Scholar
Sokolov, E.N., & Palikhova, T.N. (1999). Immediate plasticity of identifiable synapses in the land snails Helix lucorum. Acta Neurobiology Experimentalle, 59, 161–169.CrossRefGoogle ScholarPubMed
Vaitkevichius, H., Shatinskas, R., Stanikunas, R., Shvegzhda, A., & Sokolov, E.N. (in press). Kodirovanie lokal'nykh i global'nykh parametrov dvizhushchegosya stimula v zritel'noy sisteme koshki [Encoding of local and global parameters of moving stimulus in cat's visual system]. In Sokolov, E.N. & Chernorizov, A.M. (Eds.), Vektornaya psikhofiziologiya: Ot povedeniya k neyronu [Vector Psychophysiology: From Behavior to Neuron]. Moskva: Izdatel'stvo MGU.Google Scholar
Valberg, A., & Seim, Th. (2008). Neural mechanisms of chromatic and achromatic vision. Color Research & Application, 33 (6), 433–443.CrossRefGoogle Scholar
Vladusich, T., Lucassen, M.P., & Cornelissen, F.W. (2007). Brightness and darkness as perceptual dimensions. PLoS Computational Biology (PubMed Central), 3 (10), e179.CrossRefGoogle ScholarPubMed
Von Berg, E., & Shneider, G. (1972). The spectral sensitivity of the dark-adapted eye of Helix pomatia L. Journal of Vision Research, 12 (12), 2151–2152.CrossRefGoogle ScholarPubMed
Zaitseva, O.V. (1994). Strukturnaya organizatsiya sensornykh system ulitki [Structural organization of snail's sensory systems]. Zhurnal Vysshei Nervnoi Deyatel'nosti Im I.P. Pavlova, 42 (6), 1132–1150.Google Scholar
Zeki, S.M. (1983). Colour coding in the cerebral cortex: the responses of wavelength-selective and colour-coded cells in monkey visual cortex to changes in wavelength composition. Journal of Neuroscience, 9, 767–781.CrossRefGoogle ScholarPubMed
Zimachev, M.M., & Chernorizov, A.M. (2001). Struktura tsvetovogo prostranstva lyagushki v raznye periody povedencheskoy aktivnosti [Structure of frog's color space for different periods of frog's behavioral activity]. Vestnik MGU. Seriya 14. Psikhologiya, 4, 12–32.Google Scholar
Zrenner, E. (1983). Neurophysiological aspects of color vision in primates. Berlin: Springer-Verlag.CrossRefGoogle Scholar