Cellular Mechanisms of the Color Constancy in the Fish Retina

Elena M. Maximova and Vadim V. Maximov

Institute for Problems of Information Transmission,
Russian Academy of Sciences, 101447, Moscow, Russia


A paper version of the poster was presented
at the meeting in honour of John Lythgoe
"The Ecology of Vision"
Oristano, Italy (6th - 10th April, 1994)
*

Abstract. We supposed that color-coding double-opponent ganglion cells can display color constancy, for their receptive field (RF) surround might supply the center with the information about the ambient illumination, and its opponent influence on the center might well make necessary scaling for the central signals.
Responses of a certain type of color-coding ganglion cells to flat colored stimuli moving across the RF center were recorded from their axonal terminals in tectum opticum. All scene projected onto the RF was illuminated with light whose spectral composition was changed in a wide range. Under white illumination blue-green stimuli elicited OFF central response while the red ones elicited ON-OFF central response. When the RF surround was colored white, these types of responses remained unchanged while the incident light was varied from red to blue altering the spectral content of the light reflected from the stimuli. When the RF surround was covered with black velvet (i.e., in lack of information about the illumination), one could change the pattern of the central response by varying spectral composition of the illumination. Moreover, covering the surround with colored papers we transformed the pattern of the central response in a predictable manner even under white illumination. This means that the constantly illuminated surround signals the cell about the character of illumination.
Horizontal cells are known to organize the surround of the ganglion cells. Thus, owing to their prolonged polarization during illumination, horizontal cells can realize some color constancy mechanisms just at the very beginning of the visual pathway.
Preliminary reports of these findings have been made elsewhere in Russian1 and in English2.


Table of contents

Introduction

In natural environments illumination varies in a wide range, so varies spectral content of the light reflected from the objects. Nevertheless, animals do recognize surface colors correctly, irrespective of the illumination. This ability is the fundamental property of color vision known as color constancy.

One of the possible mechanisms of the color constancy consists in discounting the illumination. It requires to determine color of the prevailing illumination what visual system can do even if there is no illuminant itself in the visual field. In this case visual system uses some indirect features of the illumination. For example, it is sufficient to have some white object in the visual field to estimate the illumination color.

Mechanisms of the color constancy may be of different levels of complexity, the simplest ones, that do not need memory or learning, may be of retinal origin.

Color-coding opponent ganglion cells of the fish retina were chosen as objects for the following reasons:


Materials and Methods

Responses of retinal ganglion cells were recorded from their axonal terminals in the tectum opticum of Cyprinus carpio L. and Carassius carassius (L.)



The receptive fields (RF) of the unit was mapped by means of a flashing light-point and moving black or white spots, stripes or edges. Then, a special device to project moving stimuli into the RF was positioned at the visual field and the right projection was adjusted with a mirror.
All the scene was illuminated with two independent sources. Their intensities and spectral contents were varied in a wide range.
While investigating the color constancy stimuli (sheets of colored papers) were moved with a constant velocity across the RF center on a velvet-black background, the RF surround being covered with a stationary white or black screen. The spike activity of the unit was recorded in response to introduction (ON response) and withdrawal (OFF response) of the stimulus.


The relative efficiencies (quantum catches) of the papers under white incandescent lamp illumination were calculated for each cone type from
   spectral sensitivities of the cones,
   spectral reflectances of the papers and
   the spectrum of the illuminant.
The efficiency of perfect white diffuser was taken as 100%.

Positions of the papers relative efficiency in the cyprinid color space are shown in the RG-plane projection to the right.


Stratification of Tectal Activity





The same types and the same sequences of retinal afferents were observed in the tectum
of the pike4 and some marine5 fishes:

golden gray mullet

Liza aurata (Risso) / Mugil auratus (Risso)

wrasses

Symphodus sp. / Crenilabrus sp.

red mullet

Mullus barbatus ponticus Essipov

high-body pickarel

Spicara smaris (Linnaeus)

Black Sea scad

Trachurus mediterraneus ponticus Aleev

Properties of the detectors of vertical and horizontal lines were thoroughly investigated later and published elsewhere6,7.


General Properties of Color-Coding Units

Unlike a well-known wide variety of color-coding ganglion cells in the fish retina, only one type of color-dependent responses is recorded from retinal afferents projected into the tectum opticum.
Fig.G1 (above). Spike discharges of the color-coding unit O-16 to long-wave and short-wave light steps presented into its RF center and surround.
One can see that these responses differ a bit from the classic double color-opponent ones: there are some extra OFF-response to red illumination of the RF center and an extra ON-response to blue illumination of the RF surround.
Shown in the panel on the right side of the figure are responses represented in a graphics form. Three recordings were made for each type of stimulation in the experiment. Separate points in the space of responses correspond to different individual records, thus illustrating an experimental scatter.

Fig.G2. Spike discharges of the color-coding unit O-16 in response to introduction (ON) and withdrawal (OFF) of sheets of colored papers in its RF center.

Color-coding units receive inputs from red and green cones as revealed in color-matching experiments.

Fig.G3 (to the right). Two color-matching distribution coefficients (shown in black) obtained for the color-coding unit O-103.
The points indicate relative intensities of long-wave and short-wave lights (dashed spectral bands) in color mixtures, indistinguishable from certain monochromatic light (abscissa), the absence of reaction in response to the color substitution being a criterion of color match.

This type of retinal afferents demonstrates clear color-coding properties, their ON response being an indicator of the relative amount of a long-wave radiation in the light, reflected from the stimulus.

Fig.G4 (to the left). The correspondence between the space of responses (ON-OFF) of the color-coding unit O-43 and the RG-plane of the cyprinid color space.
Responses of the unit were recorded to presentations of various colored sheets of paper in black surround under white illumination. Dimensions of the rectangles at the figure correspond to dispersions of the experimental points. The curvilinear grid represents the distortion of the color space (see the RG-plane projection in section Materials and Methods for comparison).


Color Constancy

In lack of information about the color of the illumination (in black surround) responses of the color-coding units are determined by the light reflected from the surface presented in the RF center. So, these responses change essentially when the spectral content of the illumination varies.
When the information about the illumination is available (in white surround) the unit response keeps rather constant, it does not depend on the color of illumination and is determined exclusively by the surface color of the stimulus.

Fig.C1. Spike discharges of the color-coding unit O-16 in response to introduction (ON) and withdrawal (OFF) of sheets of colored papers in its RF center (see Fig.G2 in section General Properties of Color-Coding Units for comparison).

Fig.C2 (to the right). Cell responses to the green stimulus under white and red illumination in black and white surround.
One can see that responses change (arrow) after switching on an additional red light source, when the surround is black, and do not change, when it is white.

Fig.C3 (to the left). An increase in number of spikes in the ON response of the unit O-25 to introduction of the green stimulus into its RF center with reddening the illumination when the RF surround is black (curve 1) and the relative constancy of the response to the same stimulus when the RF surround is white (curve 2).

During these experiments, human observer also perceives the stimulus as red at large intensities of the additional red illumination, if the surround is covered with a black screen and there are no information about the illumination, but sees the stimulus as green, if the surround is white.

Fig.C4 (to the right). Experiments on simultaneous color contrast.
Under white illumination when the RF surround is covered with a green screen, ganglion cell considers the illumination to be green and responds to the gray stimulus as to the red one - its OFF-response increases. This is a well known phenomenon of simultaneous color contrast.
Opposite illusion is observed when the RF surround is covered with a red screen.

Note, that neither surrounds nor illumination change in the course of stimulation in these experiments. Only gray paper moves across the RF center on a velvet-black background.


Conclusion

Tectum opticum (with its only type of color-coding retinal afferents) is hardly the very center where color information is processed. Nevertheless, responses of the color-coding unit, recorded in the tectum, can reflect the events occurred in the retina.

Our results suggest that the pattern of response of color-coding opponent ganglion cells is not determined solely by the spectral content of the light reflected from objects presented in their RF center, but rather by the surface color of these objects, provided the information about the illumination is available. Thus, the simplest mechanisms of the color constancy exist at the retinal level.

Horizontal cells have been shown to organize the surround of the ganglion cell receptive field8. Artificial sustained polarization of the horizontal cells, as well as sustained illumination of the ganglion cell RF surround, modifies the response of the ganglion cells to stimuli presented in their RF center9. So, it is reasonable to suggest horizontal cells to be responsible for realization of some color constancy mechanisms just at the very beginning of the visual pathway.


Literature

1. E.M.Maximova, A.M.Dimentman, V.V.Maximov, O.Yu.Orlov. Electrophysiological investigation of the colour constancy in retina. In: Mechanisms of Action of the Receptor Elements of Sensory Organs - Proceedings of The 2nd All-Union Symposium on Mechanisms of Reception (Pushchino, 1971), "Nauka", Leningrad, 1973, pp. 75-80 (in Russian)

2. E.M.Maximova. Cellular mechanisms of colour constancy. (Presented at The 2nd International Congress of C.I.A.N.S. Prague, 1975), Activ. nerv. sup. (Praha), 19, 3:199-201, 1977

3. A.M.Dimentman, A.Ya.Karas, V.V.Maximov, O.Yu.Orlov. Constancy of object colour perception in Cyprinus carpio. Pavlov J. Higher Nerv. Act. 22, 4:772-779, 1972 (in Russian)

4. G.M.Zenkin, I.N.Pigarev. Detector properties of the ganglion cells in the pike retina. Biofizika 14:763-772, 1969 (in Russian)

5. E.M.Maximova, O.Yu.Orlov, A.M.Dimentman. Investigation of the visual system of some marine fishes. Voprosy Ichtiologii 11, 5:893-899, 1971 (in Russian)

6. E.M.Maximova, V.V.Maximov. Detectors of oriented lines in the visual system of the crucian carp Carassius carassius. J. evol. Biochem. & Physiol. 17, 5:519-525, 1981 (in Russian)

7. E.M.Maximova. Colour and spatial properties of detectors of oriented lines in the fish retina. Iugoslav. Physiol. Pharmacol. Acta 34, 2:351-357, 1998
The paper is available in PDF format at http://147.91.239.50/ippa/issues/34(2)/IPPA1998342_351_356.pdf (241K)

8. E.M.Maximova. Effect of intracellular polarization of horizontal cells on ganglion cell activity in the fish retina. Biofizika 14, 3:537-544, 1969 (in Russian) Translated in: Neuroscience Translations No.11, pp.114-120, 1969-1970

9. E.M.Maximova, V.V.Maximov. The role of horizontal cells in organization of ganglion cells concentric receptive fields in the fish retina. In: Visual Information Processing and Control of Motor Activity - Proceedings of the International Symposium (Sofia,1969), Bulgarian Acad. of Sci., Sofia, 1971, pp. 31-39 (in Russian)


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