- Email: [email protected]
The evolution of colour-opponent neurones and colour vision
PY.km RL-X Vol. 16. pp. 1359 10 1362. Perqamoa Press 1976. Printed in Grenr Britun.
RESEARCH NOTE THE EVOLUTION
OF COLOUR-OPPONENT AND COLOUR VISION
NEURONES
Sr~o HEMILX, TOM REUTER and KAJ VIRTANEX Department of Zoology, Division of Physiology, University of Helsinki, Arkadiank. 7, 00100 Helsinki 10, Finland (Receiced
Kq Words-retina; auratus;
15 December
1975)
ganglion cell; colour vision. Animal Classification-Carrsius
carassirls: Carussirci
Rana temporaria.
The evolution of a well developed colour vision of the type found in the gold&h (Muntz and CronlyDillon, 1966; Yager, 1967) from an animal with a single visual pigment must have involved at least the following four steps: (1) mutations producing new pigments; (2) segregation of the pigments in separate receptors; (3) formation of receptor-specitic couplings allowing two receptor types to affect some retinal neurones in an antagonistic (colour-opponent) way; (4) development of the decoding system of the brain making it possible to interpret the signals from the retina in terms of different colours. If these changes have taken place independently of each other, each of them must have provided an immediate advantage promoting its spread within the population. Some circumstances promoting the first two of these steps have recently been discussed in this journal: (1) A new visual pigment may facilitate entry into a specific photic environment by broadening the spectral sensitivity of the eye, For instance, of the two rhodopsins of the eel (AnguiJJa) with absorption peaks at 501 and 482 nm respectively, the former probably is an adaptation for fresh water and coastal marine waters and the latter for bluish ocean depths (for a sumn+y, see Beatty, 1975). (2) Referring to the idea that the evolutionary selection of multiple photopic systems, and of colour vision itself, is related to the maximization of visual contrast, McFarland and Munz (1975b) have pointed out that maximum visibility of both reflective and nonreflective objects under water requires two types of receptors, one matched to and the other offset from the spectrum of background spacelight against which the objects are detected (cf. also Lythgoe, 1968). In fact retinal extracts of a number of diurnal fishes contain binary or ternary piwent mixtures fulfilling these requirements (Munz and McFarland, 1975; McFarland and Munz, 1975a, b). The advantage of the fourth step is obvious as it allows the brain to use the colour of objects for recognizing them. Our own experimental work is focused on the third step, i.e. the colour-opponent coupling of the signals from two receptor types. We find that an addition of even a weak colour-opponent input to a retinal ganglion cell makes this responsive to
moving colour borders irrespective of the relative intensities of the two colours, i.e. the cell wiJ1 detect moving objects that have the same “bri&tness” as the background, but a different colour.
ZIETHODS
As experimental animals we used the frog (Ranu temporaria). the goldfish (Curassius auratus) and the crucian carp (Curassius carassius). We have studied the responses of single ganglion cells to moving spots of various intensities and wavelengths using an optical system, in which the light reaches the retina of the excised and opened eye through two parallel channels (for optical system and recording technique, see Donner and Reuter, 1968; Reuter, 1969). In one of the channels we have inserted a transparent screen with a dark spot, which is projected on the retina, in the other a black screen with a small hole also projected on the retina and forming a small bright field exactly covering the dark spot from the first channel. On the retina the diameter of these circular fields or “spots” is 0.35 mm. Both screens stay on the same carrier moved back and forth by a nut and screw combination driven by a motor so that the coincident spots move together over the retina with a constant speed. The background illumination from the first channel covers most of the retina and does not change during the movement. Since the wavelengths and the intensities of the &vo channels can be regulated independently by interference filters and neutral filters and wedges, the spot and the background can have any desired colour, and the spot can be either darker or brighter than the background. Action potentials were recorded extracellularly with glass micropipettes from single ganglion cells (the vitreous fluid was removed from the opened fish eyes with a sucking pipette). Series of responses were displayed on the screen of a storage oscilloscope (Tektronix D13) through the z-axis channel and photographed (Figs. 1 and 2). As the oscilloscope in this mode converts voltage amplitude into cathode-ray brightness. an action pote&al gives rise to a bright spot on the screen (at high impulse frequenties the spots tend to fuse, see Fig. 1). The row of impulses during one oscilloscope sweep corresponds to a single carrier run during which the stimulus spot crosses the receptive field of the ganglion cell. The sweep is started by a micro-switch when the carrier reaches a certain point and the stimulus spot is at a chosen distance from the center of the receptive field. All recorded responses correspond to movements in the same direction.
1359
dark
The cell was >tlmuIated
spot
with a green IBI moving spot. the red background being the same in both cases. This ~11 showed a maintained activity. i.e. in the absence of moving stimuli it generated on an average 3-7 action potentials per sec. The first and last sweeps in both IA) and (B) show this maintained actirity. The responses during the other sweeps appear both as inhibited (empty areas) and enhanced activity thigh frequency areas). In (Al the response to the bright red spot (below) indicates that the cell has a red-sensitive “on” center surrounded bq an Inhibitory region. A dark spot suppressss the acticit) in the c,-nter but gives rise to a high frequency surround response in the uppsr lzft part of Fig. X. LVhen its intensitq approaches that of the background the moving red spot has a very small effect on the spontaneous activity (arrow). ‘However. in Fig. 1B. where a green spot moves against a red background, all spot intensities produce clear responses, mainly in the form of inhibited activity. Our interpretation of Fig. ZB. based on -‘on-off stimulation of a similar cell with red and green spots, is the following: while a stimulation of the red-sensitive cones gives rise to an “on” response in the center and inhibition in the surround. a stimulation of the green-sensitive cones gives rise to a sustained inhibition in a central region con.sidernb!\~ with than the red-sensitive center (cf. Wolbarsht. Wagner and MacNichol. 1961; Daw. 1968). But since the rcd-
I
t
spot
i
10
s
I
diam.
Fig. 1. Oscilloscope recordings showinp, the responses of a crucian .carp ganglion cell to a movmg Spot crossing its receptive tieid. The abscissa is time during movement (from left to right), and as the speed was constant (1.33 mm on the retina;10 set) a certain time corresponds to a certain distance. Thus the abscissa also gives the spot diameter, i.e. the time (2.63 set) it took the spot to move a distance corresponding to its own diameter (0.35 mm). The wavelength (661 nm) and intensity (2 x lO’quanta x mm-‘sCc_’ reaching the retinal surface) of the background was kept constant. The intensity of the 657nm spot was increased between successike sweeps and was 4 log units higher during the last than during the first spot run. When the spot was much darker (above) or brighter (below) than the background its intensity increased in large steps (1 log unit both from the tirst to the second run and from the last but one to the last), but the intensity steps decreased as the spot intensity approached that of the background, and in a region including seven sweeps in the middle the intensity was increased by only 10 or 2056 per step. The arrow marks a spot run evoking no response. The spot run and its fast return took about 25 set and successive runs were started at 60 set intervals. The eye was dissected in white light and kept light-adapted during the experiments. Temperature about 11’C.
tirjt \\lth J rd
1.1) LUIJ then,
RESULTS
The strategy of our experiments is best described by referring to Fig. 1, which shows an experiment with a crucian carp ganglion cell. Stimulated as in this case with a red spot moving on a red background the receptive field of this cell had an “off’ center and “on” surround. The background intensity was kept constant, while the intensity of the spot was increased between successive sweeps being first much darker than the background (above) and finally much brighter (below). The “off’ center responded to the darkening during the passage of a dark spot, while the “on” surround on both sides responded to a bright spot. The brightest spot evoked only two action potentials, apparently because it was surrounded by some stray light affecting the antagonistic center while passing the surround. During one particular sweep (arrow) the intensity of the spot was so similar to that of the background that the cell did not react at all, nor was the red spot moving on a red background visible to a human observer (a magnified version of the stimulus is projected on a screen). Figure 2 describes an experiment with a goldfish ganglion cell having a weak colour-opponent input.
spot
diam.
Fig;. 3. Responses of a goldfish ganglion cell to moving red (A: 657 nm) and green CB:513 nm) spots against a red See bat zkground (661 nm, 2 x lo9 q x mm-’ set-‘L legsend to Fig. 1. In both (A) and (BI the first and last sweeps show maintained actilit)
1361
Research Note sensitive cones have a rather high sensitivity also to green light. and tend to dominate over the greensensitive, a very bright green spot gives rise to the same type of response as a bright red spot. Neither is there any significant difference between the responses to very dark red and green spots [second sweeps from above in (A) and (B)]. But at the intensities in between the inhibition caused by the stimulation of the green-sensitive cones is obvious. There is no clear evidence for a green-sensitive “on” region surrounding the inhibitory center, and therefore we do not know whether this cell has a complete double opponent organization of the type described by Daw (1968; red “on” center and “off’ surroundgreen “off’ center and “on” surround). It is more like Daw’s Q-cells, in which often only the center of the green-sensitive mechanism is observed. and even this is easily overpowered by the red-sensitive. We have observed very similar phenomena in the frog retina. where an unbalanced colour-opponency exists between dominating yellow-sensitive signals from the cones and easily suppressed blue-sensitive signals from the green ‘rods (Reuter and Virtanen, 1972). When tested with a yellow spot on a yellow background. the ganglion cells remain silent in the matching region, but when a blue spot on a yellow background matches the cone sensitivity, i.e. keeps the cones equally stimulated and silent, it stimulates the green rods. Thus, instead of a matching region we observe long low-frequency green rod-mediateddischarges.
It is possible that the capacity of the retina to detect colour borders preceded the capacity of the brain to distinguish between intensity and colour contrast, and it could have provided the immediate advantage needed for the establishment and further evolution of the colour-opponent organization in the retina and in the brain. Plain detection of colour borders may still be an important function for colour-opponent cells. A hint pointing in that direction is the occurrence of “concealed” colour opponency (DeMonasterio, Gouras and Tolhurst, 1975). It is a common observation that the more red-sensitive of the two colour mechanisms contributing to the responses of an opponent cell is dominating and determines the responses when strongly stimulated (Daw, 1968: goldfish; Reuter and Virtanen. 1972: frog; DeMonasterio et al.. 1975: rhesus monkey). However, when we approach the matching region of the stronger mechanism, and border detection becomes critical, the weaker gets a chance to come through. A concealed colour opponency of this type may be a method for detecting colour borders without interfering too much with the coding of brightness pattern information. Acknowledgemenrs-This work was supported by grants to K. 0. Donner and TR from the National Research Council for Sciences in Finland. We thank Prof. K. 0. Donner for important suggestions and help, and Ann-Christine Backstrom. M.Sc., for many kinds of technical assistance. REFERENCES
D1SCKSSION The first prerequisite for detecting a moving colour border irrespective of the relative intensities of the two colours is a retina with two receptor types with different spectral sensitivities. Then an intensity relation matching one of the receptors will stimulate the other. and vice versa. A further condition is, of course, that the receptors are not connected to the retinal neurones in a summating way so that a change in one type of receptor is cancelled by an opposite change in the other type [such a summation and cancelling has in fact been observed in the case of the cone and red rod signals in the frog retina (Donner and Rushton, 1959; Backstrom and Reuter, 1975)]. A colour-opponent coupling is, however, the very opposite of summation and therefore ideally suited for colour border detection (Reuter, 1969; Reuter and Virtanen, 1972). The colour-opponency of some bipolar cells in the goldfish retina seems to be due simply to the fact that the red-sensitive cones mainly stimulate them directly, but the green-sensitive only indirectly through the horizontal cells (Kaneko, 1973). Since the antagonism between direct and indirect inputs to the bipolars also serves the discrimination of intensity contrast (for a summary, see Werblin, 1974), it is probable that this system was present in the retina already when vertebrate colour vision evolved. In a retina containing two types of receptors with different visual pigments colour opponency may thus have arisen from a simple receptor specificity of the bipolar connections.
Backstrom A.-C. and Reuter T. (1975) Receptive field organization of ganglion cells in the frog retina: contributions from cones. green rods and red rods. J. Ph@ol., Lond. 246, 79-101.
Beatty D. D. (1975) Visual pigments of the American eel Anguilla rostrata. Vision Res. 15, 771-776. Daw N. W. (1968) Colour-coded ganglion cells in the goldfish retina: extension of their receptive fields by means of new stimuli. J. Physiol., Lond. 197, 567-592. DeMonasterio F. M., Gouras P. and Tolhurst D. J. (1975) Concealed colour opponency in ganglion cells of the rhesus monkev retina. J. Phvsiol.. Lond. 251. X7-229. Donner K. 0. and Reuter T. (1968) Visual adaptation of the rhodopsin rods in the frog’s retina. J. Phpiol., Lond. 199, 59-87.
Donner K. 0. and Rushton W. A. H. (1959) Retinal stimulation by light substitution. J. Physiol., Lond. 149, 288-302.
Kaneko A. (1973) Receptive field organization of bipolar and amacrine cells in the goldfish retina. J. Physiol., Lond. 235, 133-153. Lythgoe J. N. (1968) Visual pigments and visual range underwater. Vision Res. 8, 997-1012. McFarland W. N. and Munz F. W. (19758) Part II: the
photic environment of clear tropical seas during the day. Vision Res. 15, 1063-1070. McFarland W. N. and Munz F. W. (1975b) Part III: the evolution of photopic visual pigments in fishes. Vision Res. 13, 1071-1080.
Muntz W. R. A. and Cronly-Dillon J. R. (1966) Colour discrimination in goldfish. Anim Behac. 14, 351-355. Munz F. W. and McFarland W. N. (1975) Part I: presumptive cone pigments extracted from tropical marine fishes. Vision Res. 15, 1045-1062. Reuter T. (1969) Visual pigments and ganglion cell activity in the retinae of tadpoles and adult frogs (Rann remporaria L.). Acta :ool. fenn. 122. l-64.
1363
Research Sotr
Reutrr T. and Vtrtanen R. (1972) Border and colour coding in the retina of the frog. .~arurr. Lon‘l. 139. X0-263. Werblin F. S. (19i4) Control of retinal sensitivity. II. Lateral interactions at the outer plexiform lqsr J. yzn. Ph.sio[. 63. 61X7. Wolbarsht M. L.. Wagner H. G. and MacNichol E. F.. Jr. (1961) Receptive fields of retinal ganglion cells: extent
and jpectral jensitl\ttq-. In T/I< i ;,ud Z~st~m:.Ierc~(Edited by Jung R. and Komhuber H.). pp. 1’0-175. Springer. Berlin. Yager D. 11967) Behaiiorsl measures and theoretlcsl analysis of jpectral jensitl\ity and spectral saturation in the goldfish, C[iruss&s ~lurutw. C’ision Rrr. 7, 707-717. ph~siolog.~ unrl Psyhophys~s
RESEARCH NOTE THE EVOLUTION
OF COLOUR-OPPONENT AND COLOUR VISION
NEURONES
Sr~o HEMILX, TOM REUTER and KAJ VIRTANEX Department of Zoology, Division of Physiology, University of Helsinki, Arkadiank. 7, 00100 Helsinki 10, Finland (Receiced
Kq Words-retina; auratus;
15 December
1975)
ganglion cell; colour vision. Animal Classification-Carrsius
carassirls: Carussirci
Rana temporaria.
The evolution of a well developed colour vision of the type found in the gold&h (Muntz and CronlyDillon, 1966; Yager, 1967) from an animal with a single visual pigment must have involved at least the following four steps: (1) mutations producing new pigments; (2) segregation of the pigments in separate receptors; (3) formation of receptor-specitic couplings allowing two receptor types to affect some retinal neurones in an antagonistic (colour-opponent) way; (4) development of the decoding system of the brain making it possible to interpret the signals from the retina in terms of different colours. If these changes have taken place independently of each other, each of them must have provided an immediate advantage promoting its spread within the population. Some circumstances promoting the first two of these steps have recently been discussed in this journal: (1) A new visual pigment may facilitate entry into a specific photic environment by broadening the spectral sensitivity of the eye, For instance, of the two rhodopsins of the eel (AnguiJJa) with absorption peaks at 501 and 482 nm respectively, the former probably is an adaptation for fresh water and coastal marine waters and the latter for bluish ocean depths (for a sumn+y, see Beatty, 1975). (2) Referring to the idea that the evolutionary selection of multiple photopic systems, and of colour vision itself, is related to the maximization of visual contrast, McFarland and Munz (1975b) have pointed out that maximum visibility of both reflective and nonreflective objects under water requires two types of receptors, one matched to and the other offset from the spectrum of background spacelight against which the objects are detected (cf. also Lythgoe, 1968). In fact retinal extracts of a number of diurnal fishes contain binary or ternary piwent mixtures fulfilling these requirements (Munz and McFarland, 1975; McFarland and Munz, 1975a, b). The advantage of the fourth step is obvious as it allows the brain to use the colour of objects for recognizing them. Our own experimental work is focused on the third step, i.e. the colour-opponent coupling of the signals from two receptor types. We find that an addition of even a weak colour-opponent input to a retinal ganglion cell makes this responsive to
moving colour borders irrespective of the relative intensities of the two colours, i.e. the cell wiJ1 detect moving objects that have the same “bri&tness” as the background, but a different colour.
ZIETHODS
As experimental animals we used the frog (Ranu temporaria). the goldfish (Curassius auratus) and the crucian carp (Curassius carassius). We have studied the responses of single ganglion cells to moving spots of various intensities and wavelengths using an optical system, in which the light reaches the retina of the excised and opened eye through two parallel channels (for optical system and recording technique, see Donner and Reuter, 1968; Reuter, 1969). In one of the channels we have inserted a transparent screen with a dark spot, which is projected on the retina, in the other a black screen with a small hole also projected on the retina and forming a small bright field exactly covering the dark spot from the first channel. On the retina the diameter of these circular fields or “spots” is 0.35 mm. Both screens stay on the same carrier moved back and forth by a nut and screw combination driven by a motor so that the coincident spots move together over the retina with a constant speed. The background illumination from the first channel covers most of the retina and does not change during the movement. Since the wavelengths and the intensities of the &vo channels can be regulated independently by interference filters and neutral filters and wedges, the spot and the background can have any desired colour, and the spot can be either darker or brighter than the background. Action potentials were recorded extracellularly with glass micropipettes from single ganglion cells (the vitreous fluid was removed from the opened fish eyes with a sucking pipette). Series of responses were displayed on the screen of a storage oscilloscope (Tektronix D13) through the z-axis channel and photographed (Figs. 1 and 2). As the oscilloscope in this mode converts voltage amplitude into cathode-ray brightness. an action pote&al gives rise to a bright spot on the screen (at high impulse frequenties the spots tend to fuse, see Fig. 1). The row of impulses during one oscilloscope sweep corresponds to a single carrier run during which the stimulus spot crosses the receptive field of the ganglion cell. The sweep is started by a micro-switch when the carrier reaches a certain point and the stimulus spot is at a chosen distance from the center of the receptive field. All recorded responses correspond to movements in the same direction.
1359
dark
The cell was >tlmuIated
spot
with a green IBI moving spot. the red background being the same in both cases. This ~11 showed a maintained activity. i.e. in the absence of moving stimuli it generated on an average 3-7 action potentials per sec. The first and last sweeps in both IA) and (B) show this maintained actirity. The responses during the other sweeps appear both as inhibited (empty areas) and enhanced activity thigh frequency areas). In (Al the response to the bright red spot (below) indicates that the cell has a red-sensitive “on” center surrounded bq an Inhibitory region. A dark spot suppressss the acticit) in the c,-nter but gives rise to a high frequency surround response in the uppsr lzft part of Fig. X. LVhen its intensitq approaches that of the background the moving red spot has a very small effect on the spontaneous activity (arrow). ‘However. in Fig. 1B. where a green spot moves against a red background, all spot intensities produce clear responses, mainly in the form of inhibited activity. Our interpretation of Fig. ZB. based on -‘on-off stimulation of a similar cell with red and green spots, is the following: while a stimulation of the red-sensitive cones gives rise to an “on” response in the center and inhibition in the surround. a stimulation of the green-sensitive cones gives rise to a sustained inhibition in a central region con.sidernb!\~ with than the red-sensitive center (cf. Wolbarsht. Wagner and MacNichol. 1961; Daw. 1968). But since the rcd-
I
t
spot
i
10
s
I
diam.
Fig. 1. Oscilloscope recordings showinp, the responses of a crucian .carp ganglion cell to a movmg Spot crossing its receptive tieid. The abscissa is time during movement (from left to right), and as the speed was constant (1.33 mm on the retina;10 set) a certain time corresponds to a certain distance. Thus the abscissa also gives the spot diameter, i.e. the time (2.63 set) it took the spot to move a distance corresponding to its own diameter (0.35 mm). The wavelength (661 nm) and intensity (2 x lO’quanta x mm-‘sCc_’ reaching the retinal surface) of the background was kept constant. The intensity of the 657nm spot was increased between successike sweeps and was 4 log units higher during the last than during the first spot run. When the spot was much darker (above) or brighter (below) than the background its intensity increased in large steps (1 log unit both from the tirst to the second run and from the last but one to the last), but the intensity steps decreased as the spot intensity approached that of the background, and in a region including seven sweeps in the middle the intensity was increased by only 10 or 2056 per step. The arrow marks a spot run evoking no response. The spot run and its fast return took about 25 set and successive runs were started at 60 set intervals. The eye was dissected in white light and kept light-adapted during the experiments. Temperature about 11’C.
tirjt \\lth J rd
1.1) LUIJ then,
RESULTS
The strategy of our experiments is best described by referring to Fig. 1, which shows an experiment with a crucian carp ganglion cell. Stimulated as in this case with a red spot moving on a red background the receptive field of this cell had an “off’ center and “on” surround. The background intensity was kept constant, while the intensity of the spot was increased between successive sweeps being first much darker than the background (above) and finally much brighter (below). The “off’ center responded to the darkening during the passage of a dark spot, while the “on” surround on both sides responded to a bright spot. The brightest spot evoked only two action potentials, apparently because it was surrounded by some stray light affecting the antagonistic center while passing the surround. During one particular sweep (arrow) the intensity of the spot was so similar to that of the background that the cell did not react at all, nor was the red spot moving on a red background visible to a human observer (a magnified version of the stimulus is projected on a screen). Figure 2 describes an experiment with a goldfish ganglion cell having a weak colour-opponent input.
spot
diam.
Fig;. 3. Responses of a goldfish ganglion cell to moving red (A: 657 nm) and green CB:513 nm) spots against a red See bat zkground (661 nm, 2 x lo9 q x mm-’ set-‘L legsend to Fig. 1. In both (A) and (BI the first and last sweeps show maintained actilit)
1361
Research Note sensitive cones have a rather high sensitivity also to green light. and tend to dominate over the greensensitive, a very bright green spot gives rise to the same type of response as a bright red spot. Neither is there any significant difference between the responses to very dark red and green spots [second sweeps from above in (A) and (B)]. But at the intensities in between the inhibition caused by the stimulation of the green-sensitive cones is obvious. There is no clear evidence for a green-sensitive “on” region surrounding the inhibitory center, and therefore we do not know whether this cell has a complete double opponent organization of the type described by Daw (1968; red “on” center and “off’ surroundgreen “off’ center and “on” surround). It is more like Daw’s Q-cells, in which often only the center of the green-sensitive mechanism is observed. and even this is easily overpowered by the red-sensitive. We have observed very similar phenomena in the frog retina. where an unbalanced colour-opponency exists between dominating yellow-sensitive signals from the cones and easily suppressed blue-sensitive signals from the green ‘rods (Reuter and Virtanen, 1972). When tested with a yellow spot on a yellow background. the ganglion cells remain silent in the matching region, but when a blue spot on a yellow background matches the cone sensitivity, i.e. keeps the cones equally stimulated and silent, it stimulates the green rods. Thus, instead of a matching region we observe long low-frequency green rod-mediateddischarges.
It is possible that the capacity of the retina to detect colour borders preceded the capacity of the brain to distinguish between intensity and colour contrast, and it could have provided the immediate advantage needed for the establishment and further evolution of the colour-opponent organization in the retina and in the brain. Plain detection of colour borders may still be an important function for colour-opponent cells. A hint pointing in that direction is the occurrence of “concealed” colour opponency (DeMonasterio, Gouras and Tolhurst, 1975). It is a common observation that the more red-sensitive of the two colour mechanisms contributing to the responses of an opponent cell is dominating and determines the responses when strongly stimulated (Daw, 1968: goldfish; Reuter and Virtanen. 1972: frog; DeMonasterio et al.. 1975: rhesus monkey). However, when we approach the matching region of the stronger mechanism, and border detection becomes critical, the weaker gets a chance to come through. A concealed colour opponency of this type may be a method for detecting colour borders without interfering too much with the coding of brightness pattern information. Acknowledgemenrs-This work was supported by grants to K. 0. Donner and TR from the National Research Council for Sciences in Finland. We thank Prof. K. 0. Donner for important suggestions and help, and Ann-Christine Backstrom. M.Sc., for many kinds of technical assistance. REFERENCES
D1SCKSSION The first prerequisite for detecting a moving colour border irrespective of the relative intensities of the two colours is a retina with two receptor types with different spectral sensitivities. Then an intensity relation matching one of the receptors will stimulate the other. and vice versa. A further condition is, of course, that the receptors are not connected to the retinal neurones in a summating way so that a change in one type of receptor is cancelled by an opposite change in the other type [such a summation and cancelling has in fact been observed in the case of the cone and red rod signals in the frog retina (Donner and Rushton, 1959; Backstrom and Reuter, 1975)]. A colour-opponent coupling is, however, the very opposite of summation and therefore ideally suited for colour border detection (Reuter, 1969; Reuter and Virtanen, 1972). The colour-opponency of some bipolar cells in the goldfish retina seems to be due simply to the fact that the red-sensitive cones mainly stimulate them directly, but the green-sensitive only indirectly through the horizontal cells (Kaneko, 1973). Since the antagonism between direct and indirect inputs to the bipolars also serves the discrimination of intensity contrast (for a summary, see Werblin, 1974), it is probable that this system was present in the retina already when vertebrate colour vision evolved. In a retina containing two types of receptors with different visual pigments colour opponency may thus have arisen from a simple receptor specificity of the bipolar connections.
Backstrom A.-C. and Reuter T. (1975) Receptive field organization of ganglion cells in the frog retina: contributions from cones. green rods and red rods. J. Ph@ol., Lond. 246, 79-101.
Beatty D. D. (1975) Visual pigments of the American eel Anguilla rostrata. Vision Res. 15, 771-776. Daw N. W. (1968) Colour-coded ganglion cells in the goldfish retina: extension of their receptive fields by means of new stimuli. J. Physiol., Lond. 197, 567-592. DeMonasterio F. M., Gouras P. and Tolhurst D. J. (1975) Concealed colour opponency in ganglion cells of the rhesus monkev retina. J. Phvsiol.. Lond. 251. X7-229. Donner K. 0. and Reuter T. (1968) Visual adaptation of the rhodopsin rods in the frog’s retina. J. Phpiol., Lond. 199, 59-87.
Donner K. 0. and Rushton W. A. H. (1959) Retinal stimulation by light substitution. J. Physiol., Lond. 149, 288-302.
Kaneko A. (1973) Receptive field organization of bipolar and amacrine cells in the goldfish retina. J. Physiol., Lond. 235, 133-153. Lythgoe J. N. (1968) Visual pigments and visual range underwater. Vision Res. 8, 997-1012. McFarland W. N. and Munz F. W. (19758) Part II: the
photic environment of clear tropical seas during the day. Vision Res. 15, 1063-1070. McFarland W. N. and Munz F. W. (1975b) Part III: the evolution of photopic visual pigments in fishes. Vision Res. 13, 1071-1080.
Muntz W. R. A. and Cronly-Dillon J. R. (1966) Colour discrimination in goldfish. Anim Behac. 14, 351-355. Munz F. W. and McFarland W. N. (1975) Part I: presumptive cone pigments extracted from tropical marine fishes. Vision Res. 15, 1045-1062. Reuter T. (1969) Visual pigments and ganglion cell activity in the retinae of tadpoles and adult frogs (Rann remporaria L.). Acta :ool. fenn. 122. l-64.
1363
Research Sotr
Reutrr T. and Vtrtanen R. (1972) Border and colour coding in the retina of the frog. .~arurr. Lon‘l. 139. X0-263. Werblin F. S. (19i4) Control of retinal sensitivity. II. Lateral interactions at the outer plexiform lqsr J. yzn. Ph.sio[. 63. 61X7. Wolbarsht M. L.. Wagner H. G. and MacNichol E. F.. Jr. (1961) Receptive fields of retinal ganglion cells: extent
and jpectral jensitl\ttq-. In T/I< i ;,ud Z~st~m:.Ierc~(Edited by Jung R. and Komhuber H.). pp. 1’0-175. Springer. Berlin. Yager D. 11967) Behaiiorsl measures and theoretlcsl analysis of jpectral jensitl\ity and spectral saturation in the goldfish, C[iruss&s ~lurutw. C’ision Rrr. 7, 707-717. ph~siolog.~ unrl Psyhophys~s